Size variation and cell proliferation in chemosensory brain areas of a lizard (Podarcis hispanica): Effects of sex and season

European Journal of Neuroscience

Volumn 28, Issue 1, 2008, Pages 87-98

  Sampedro, Carlos ^a   Font, Enrique ^a   Desfilis, Ester ^b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Adult neurogenesis; Chemoreception; Reptiles; Seasonality; Sexual dimorphism

Indexed keywords

BROXURIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY SIZE; BRAIN CORTEX; BREEDING; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; LIZARD; MALE; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; SEASONAL VARIATION; SEX DIFFERENCE; ANIMAL; BRAIN; HISTOLOGY; ODOR; ORGAN SIZE; PHYSIOLOGY; SEASON; SEXUAL DEVELOPMENT;

ANIMALS; BRAIN; CELL PROLIFERATION; FEMALE; LIZARDS; MALE; OLFACTORY BULB; ORGAN SIZE; SEASONS; SEX CHARACTERISTICS; SEX FACTORS; SMELL;

EID: 54049140060     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06287.x     Document Type: Article

References (87)

1. Ampatzis, K. & Dermon, C.R. (2007) Sex differences in adult cell proliferation within the zebrafish (Danio rerio) cerebellum. Eur. J. Neurosci., 25, 1030-1040.
2. Ball, G.F. & MacDougall-Shackleton, S.A. (2001) Sex differences in songbirds
3. years later: what have we learned and where do we go? Microsc. Res. Tech., 54, 327-334.
4. Barbosa, D., Font, E., Desfilis, E. & Carretero, M.A. (2006) Chemically mediated species recognition in closely related Podarcis wall lizards. J. Chem. Ecol, 32, 1587-1598.
5. Barnea, A. & Nottebohm, F. (1994) Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc. Natl Acad. Sci. USA, 91, 11217-11221.
6. Brown, J.P., Couillard-Despres, S., Cooper-Kuhn, C.M., Winkler, J., Aigner, L. & Kuhn, H.G. (2003) Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol., 467, 1-10.
7. Carazo, P., Font, E. & Desfilis, E. (2007) Chemosensory assessment of rival competitive ability and scent mark function in a lizard (Podarcis hispanica). Anim. Behav., 74, 895-902.
8. Cooke, B., Hegstrom, C.D., Villeneuve, L.S. &Breedlove, S.M. (1998) Sexual differentiation of the vertebrate brain: principles and mechanisms. Front. Neuroendocrinol., 19, 323-362.
9. Cooper, W.E. (1996) Preliminary reconstructions of nasal chemosensory evolution in Squamata. Amphib.-Reptil., 17, 395-415.
10. Cooper, W.E. & Perez-Mellado, V. (2002) Pheromonal discriminations of sex, reproductive condition, and species by the lacertid lizard Podarcis hispanica. J. Exp. Zool., 292, 523-527.
11. Cox, R.M., Butler, M.A. & John-Alder, H.B. (2007). The evolution of sexual dimorphism in reptiles. In Fairbairn, D.J., Blanckenhorn, W.U. & Szekely, T. (Eds), Sex, Size &Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, Oxford, UK, pp. 38-49.
12. Crews, D., Wade, J. & Wilczynski, W. (1990) Sexually dimorphic areas in the brain of whiptail lizards. Brain Behav. Evol., 36, 262-270. Crews, D., Robker, R. & Mendonca, M. (1993) Seasonal fluctuations in brain nuclei in the red-sided garter snake and their hormonal control. J. Neurosci., 13, 5356-5364.
13. Dawley, E.M., Fingerlin, A., Hwang, D., John, S.S. & Stankiewicz, C.A. (2000) Seasonal cell proliferation in the chemosensory epithelium and brain of red-backed salamanders, Plethodon cinereus. Brain Behav. Evol., 56, 1-13.
14. Dawley, E.M., Nelsen, M., Lopata, A., Schwartz, J. & Bierly, A. (2006) Cell birth and survival following seasonal periods of cell proliferation in the chemosensory epithelia of red-backed salamanders, Plethodon cinereus. Brain Behav. Evol., 68, 26-36.
15. Desfilis, E., Font, E. & Guillen-Salazar, F. (2003) Stimulus control of predatory behavior by the Iberian wall lizard (Podarcis hispanica, Sauria, Lacertidae): effects of familiary with prey. J. Comp. Psychol., 117, 309-316.
16. Font, E. & Desfilis, E. (2002) Chemosensory recognition of familiar and unfamiliar conspecifics by juveniles of the Iberian wall lizard (Podarcis hispanica). Ethology, 108, 319-330.
17. Font, E. & Schwartz, J.M. (1989) Ketamine as an anesthetic for some squamate reptiles. Copeia, 1989, 484-486.
18. Font, E., Desfilis, E., Perez-Canellas, M.M. & Garcia-Verdugo, J.M. (2001) Neurogenesis and neuronal regeneration in the adult reptilian brain. Brain Behav. Evol., 58, 276-295.
19. Galea, L.A. (2008) Gonadal hormone modulation ofneurogenesis in the dentate gyrus of adult male and female rodents. Brain Res. Rev., 57, 332-341.
20. Galea, L.A. & McEwen, B.S. (1999) Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience, 89, 955-964.
21. Gheusi, G., Cremer, H., McLean, H., Chazal, G., Vincent, J. & Lledo, P.M. (2000) Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl Acad. Sci. USA, 97, 1823-1828.
22. Gleeson, J.G., Lin, P.T., Flanagan, L.A. & Walsh, C.A. (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23, 257-271.
23. Godwin, J. & Crews, D. (1997) Sex differences in the nervous system of reptiles. Cell. Mol. Neurobiol., 17, 649-669.
24. Godwin, J. & Crews, D. 2002. Hormones, brain and behavior in reptiles. In Pfaff, D.W., Arnold, A., Etgen, A., Fahrbach, S., Moss, R. &Rubin, R. (Eds), Hormones, Brain and Behavior. Academic Press, New York, pp. 545-585.
25. Gomez, M., Font, E. & Desfilis, E. 1993. Chemoreception in the Lacertidae: exploration and conspecific discrimination in the Spanish wall lizard, Podarcis hispanica. In Valakos, E.D., Bohme, W., Perez-Mellado, V. & Maragou, P. (Eds), Lacertids in the Mediterranean Region: A Biological Approach. Hellenic Zoological Society, Athens, Greece, pp. 213-230.
26. Gonzalez-Granero, S., Desfilis, E. & Garcia-Verdugo, J. M. (2006) Does tangential migration to olfactory bulbs exist in lizards? FENS Forum Abstracts, Vol. 3, A015.9. 5th FENS Forum of European Neuroscience, Vienna, Austria, July 8-12.
27. 3H]testosterone localization in the brains of garter snakes: an autoradiographic study. Gen. Comp. Endocrinol., 46, 211-224.
28. Hamdani, H., Lastein, S., Gregersen, F. & D0ving, K.B. (2008) Seasonal variations in olfactory sensory neurons - fish sensitivity to sex pheromones explained? Chem. Senses, 33, 119-123.
29. Healy, S. & Guilford, T. (1990) Olfactory-bulb size and nocturnality in birds. Evolution, 44, 339-346.
30. Healy, S. & Rowe, C. (2007) A critique of comparative studies of brain size. Proc. Roy. Soc. B, 274, 453-464.
31. Hildebrand, J.G. & Shepherd, G.M. (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci., 20, 595-631.
32. Holmes, M.M., Bartrem, C.L. & Wade, J. (2007) Androgen dependent seasonal changes in muscle fiber type in the dewlap neuromuscular system of green anoles. Physiol. Behav., 91, 601-608.
33. Hoshooley, J.S. & Sherry, D.F. (2004) Neuron production, neuron number, and structure size are seasonally stable in the hippocampus of the food-storing black-capped chickadee (Poecile atricapillus). Behav. Neurosci., 118, 345-355.
34. Hoshooley, J.S., Phillmore, L.S., Sherry, D.F. & MacDougall- Shackleton, S.A. (2007) Annual cycle of the black-capped chickadee: seasonality of food- storing and the hippocampus. Brain Behav. Evol., 69, 161-168.
35. Kabelik, D., Weiss, S.L. & Moore, M.C. (2006) Steroid hormone mediation of limbic brain plasticity and aggression in free-living tree lizards, Urosaurus ornatus. Horm. Behav., 49, 587-597.
36. Kabelik, D., Weiss, S.L. & Moore, M.C. (2008) Steroid hormones alter neuroanatomy and aggression independently in the tree lizard. Physiol. Behav., 93, 492-501.
37. Lavenex, P., Steele, M.A. & Jacobs, L.F. (2000a) Sex differences, but no seasonal variations in the hippocampus of food-caching squirrels: a stereological study. J. Comp. Neurol., 425, 152-166.
38. Lavenex, P., Steele, M.A. & Jacobs, L.F. (2000b) The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels. Eur. J. Neurosci., 12, 643-648.
39. Lazzari, M. & Franceschini, V. (2001) Glial fibrillary acidic protein and vimentin immunoreactivity of astroglial cells in the nervous system of adult Podarcis sicula (Squamata, Lacertidae). J. Anat., 198, 67-75.
40. Legendre, P. & Legendre, L. 1998. Numerical Ecology. Elsevier Science, Amsterdam.
41. Leitner, S., Voigt, C., Garcia-Segura, L.M., Van't Hof, T. & Gahr, M. (2001) Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas. Horm. Behav., 40, 160-168.
42. Lovern, M.B., Holmes, M.M, Fuller, C.O. & Wade, J. (2004) Effects of testosterone on the development of neuromuscular systems and their target tissues involved in courtship and copulation in green anoles (Anolis carolinensis). Horm. Behav., 45, 295-305.
43. Mansfield, J.H., Quan, W., Jia, C. & Halpern, M. (2005) Sexual dimorphism in the accessory olfactory bulb and vomeronasal organ of the gray short-tailed opossum, Monodelphis domestica. In Mason, R.T., LeMaster, M.P. & Muller-Schwarze, D. (Eds), Chemical Signals in Vertebrates, Vol. 10. Springer, New York, pp. 283-290.
44. Meisami, E. (1989) A proposed relationship between increases in the number of olfactory receptor neurons, convergence ratio and sensitivity in the developing rat. Dev. Brain Res., 46, 9-19.
45. Nordeen, E.J. & Nordeen, K.W. (1988) Sex and regional differences in the incorporation of neurons born during song learning in zebra finches. J. Neurosci., 8, 2869-2874.
46. Nottebohm, F. (1981) A brain for all seasons: cyclical anatomical changes insong control nuclei of the canary brain. Science, 214, 1368-1370.
47. O'Bryant, E.L. & Wade, J. (1999) Sexual dimorphisms in a neuromuscular system regulating courtship in the green anole lizard: effects of season and androgen treatment. J. Neurobiol., 40, 202-213.
48. O'Bryant, E.L. & Wade, J. (2002) Seasonal and sexual dimorphisms in the green anole forebrain. Horm. Behav., 41, 384-395.
49. Ormerod, B.K. & Galea, L.A. (2001) Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: a possible regulatory role for estradiol. Neuroscience, 102, 369-379.
50. Ormerod, B.K. & Galea, L.A. (2003) Reproductive status influences the survival of new cells in the dentate gyrus of adult male meadow voles. Neurosci. Lett., 2003, 25-28.
51. Packard, G.C. & Boardman, T.J. (1999) The use of percentages and size- specific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comp. Biochem. Physiol. A, 122, 37-44.
52. Peretto, P., Giachino, C., Panzica, G.C. & Fasolo, A. (2001) Sexually dimorphic neurogenesis is topographically matched with the anterior accessory olfactory bulb of the adult rat. Cell Tissue Res., 306, 385-389.
53. Perez-Mellado, V. (1982) Algunos datos sobre la reproduccion de dos especies de Lacertidae (Sauria, Reptilia) en el Sistema Central. Bol. R. Soc. Esp. Hist. Nat. Secc. Biol., 80, 165-173.
54. Perez-Mellado, V. (1997) Genus Podarcis. In Salvador, A. et al. (Eds), Reptiles. Fauna Iberica, Vol. 10. Museo Nacional de Ciencias Naturales (CSIC), Madrid, pp 242-306.
55. Platel, R. (1974) Poids encephalique et indice d'encephalisation chez les reptiles sauriens. Zool. Anz., 192, 332-382.
56. Platel, R. (1975) Encephalization and sex among Squamata. Bull. Soc. Zool. France, 100, 621-631.
57. Pucek, M. (1965) Water content and seasonal changes of the brain-weight in shrews. Acta Theriol., 10, 353-367.
58. Quinn, G.P. & Keough, M.J. 2002. Experimental Design and Data Analysis for
59. Biologists. Cambridge University Press, Cambridge.
60. Ramírez-Castillejo, C., Nacher, J., Molowny, A., Ponsoda, X. & López-García, 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.
61. Rasika, S., Nottebohm, F. & Álvarez-Buylla, A. (1994) Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc. Natl Acad. Sci. USA, 91, 7854-7858.
62. Rhen, T. & Crews, D. (2001) Distribution of androgen and estrogen receptor mRNA in the brain and reproductive tissues of the leopard gecko, Eublepharis macularius. J. Comp. Neurol., 437, 385-397.
63. Rochefort, C., Gheusi, G., Vincent, J.D. &Lledo, P.M. (2002) Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci., 22, 2679-2689.
64. Roth, E.D., Lutterschmidt, W.I. & Wilson, D.A. (2006) Relative medial and dorsal cortex volume in relation to sex differences in spatial ecology of a snake population. Brain Behav. Evol., 67, 103-110.
65. Ruiz, C.C. &Wade, J. (2002) Sexual dimorphisms in a copulatory neuromuscular system in the green anole lizard. J. Comp. Neurol., 443, 289-297.
66. Salom, S., Font, C. & Martinez-Garcia, F. (1994) Seasonal sexually dimorphic distribution of neuropeptide Y-like immunoreactive neurons in the forebrain of the lizard Podarcis hispanica. J. Chem. Neuroanat., 7, 217-225.
67. Schwenk, K. (1993) The evolution of chemoreception in squamate reptiles: a phylogenetic approach. Brain Behav. Evol., 41, 124-137.
68. Segovia, S. & Guillamon, A. (1993) Sexual dimorphism in the vomeronasal pathway and sex differences in reproductive behaviors. Brain Res. Rev., 18, 51-74.
69. Segovia, S., Orensanz, L.M., Valencia, A. & Guillamon, A. (1984) Effects of sex steroids on the development of the accessory olfactory bulb in the rat: a volumetric study. Brain Res., 318, 312-314.
70. Segovia, S., Garcia-Falgueras, A., Carrillo, B., Collado, P., Pinos, H., Perez-Laso, C., Vinader-Caerols, C., Beyer, C. & Guillamon, A. (2006) Sexual dimorphism in the vomeronasal system of the rabbit. Brain Res., 1102, 52-62.
71. Simerly, R.B. (2002) Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci., 25, 507-536.
72. Smulders, T.V., Shiflett, M.W., Sperling, A.J. & DeVoogd, T.J. (2000) Seasonal changes in neuron numbers in the hippocampal formation ofa food-hoarding bird: the black-capped chickadee. J. Neurobiol., 44, 414-422.
73. Sokal, R.R. & Rohlf, F.J. 1995. Biometry - The Principles and Practice of Statistics in Biological Research, 3rd Edn. WH Freeman, New York.
74. Stoll, C.J. & Voorn, P. (1985) The distribution of hypothalamic and extrahypothalamic vasotocinergic cells and fibers in the brain of a lizard, Gecko gekko: presence of a sex difference. J. Comp. Neurol., 239, 193-204.
75. Striedter, G.F. 2005. Principles ofBrain Evolution. Sinauer, Sunderland, MA.
76. Tai, F.D., Wang, T.Z., Zhang, Y.H. & Sun, R.Y. (2004) Sexual dimorphism of the vomeronasal organ and the accessory olfactory bulb of the mandarin vole Microtus mandarinus and the reed vole M. fortis. Acta Theriol., 49, 33-42.
77. Tanapat, P., Hastings, N.B., Reeves, A. & Gould, E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus ofthe adult female rat. J. Neurosci., 19, 5792-5801.
78. Tramontin, A.D. & Brenowitz, E.A. (2000) Seasonal plasticity in the adult brain. Trends Neurosci., 23, 251-258.
79. Van Damme, R. & Castilla, A.M. (1996) Chemosensory predator recognition in the lizard Podarcis hispanica: effects of predation pressure relaxation. J. Chem. Ecol, 22, 13-22.
80. Wade, J. (1998) Sexual dimorphisms in the brainstem ofthe green anole lizard. Brain Behav. Evol., 52, 46-54.
81. Wade, J. & Crews, D. (1991) The relationship between reproductive state and "sexually" dimorphic brain areas in sexually reproducing and parthenoge- netic whiptail lizards. J. Comp. Neurol., 309, 507-514.
82. Waters, P., Woodley, S.K. & Baum, M.J. (2005) Sex difference in the distribution and size of glomeruli in the ferret's main olfactory bulb. Neurosci. Lett., 381, 237-241.
83. Weiler, E (1992) Seasonal changes in adult mammalian brain weight. Naturwissenschaften, 79, 474-476.
84. Weiler, E., Apfelbach, R. & Farbman, A. I. (1999) The vomeronasal organ of the male ferret. Chem. Senses, 24, 127-136.
85. Weruaga, E., Briñón, J.G., Porteros, A., Arévalo, R., Aijo´n, J. & Alonso, J.R. (2001) A sexually dimorphic group of atypical glomeruli in the mouse olfactory bulb. Chem. Senses, 26, 7-15.
86. Yaskin, V. A. (1994) Variation in the brain morphology of the common shrew. in Merritt, J. F., Kirkland Jr, G. L. &Rose, R. K. (Eds), Advances in the Biology of Shrews, Vol 18. Special Publication Carnegie Museum of Natural History, Pittsburgh, PA, pp. 155-161.
87. Zikopoulos, B., Kentouri, M. & Dermon, C.R. (2001) Cell genesis in the hypothalamus is associated to the sexual phase of a hermaphrodite teleost. NeuroReport, 12, 2477-2481.