Changes in neurogenesis with post‑hatching age in the male Japanese quail (Cortunix japonica) brain

• Autorzy: Nkomozepi P. , Mazengenya P. , Ihunwo A.O.
• Języki publikacji: EN

Abstrakty

EN

Most avian neurogenesis studies have previously focused on the song control system and little attention has been given to non-song birds. The objective of this study was to assess changes in neurogenesis associated with post-hatching age (3-12 weeks) in the Japanese quail brain using proliferating cell nuclear antigen (PCNA) and doublecortin (DCX) immunohistochemistry. PCNA-immunoreactive (ir) cells were observed mainly in the olfactory bulb ventricular zone, telencephalic ventricular zones and cerebellum. Fewer PCNA-ir cells were also observed in the hypothalamus, thalamus and bed nucleus of the stria terminalis. In telencephalic ventricular zones, PCNA-ir cells were concentrated ventrally and dorsally adjacent to the mesopallium and medial striatum, respectively. DCX-ir cells were observed in the olfactory bulb, telencephalon and cerebellum. Furthermore, DCX-ir cells were scattered throughout the pallium except in the entopallium and arcopallium, septal nuclei and striatum. Fewer DCX-ir cells were also observed in the hippocampus and bed nucleus of stria terminalis. The density of PCNA-ir cells and DCX-ir cells in all brain areas declined with post-hatching age. In conclusion, cell proliferation appears to be restricted to the ventricular zones whereas neuronal recruitment is more widespread in the olfactory bulb, telencephalon and cerebellum. Postnatal neuronal incorporation appears to be absent in the diencephalon and mesencephalon.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2018
• Tom: 78
• Numer: 2
• Opis fizyczny: p.173-186,fig.,ref.

Twórcy

autor

Nkomozepi P.

• School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
• Department of Human Anatomy and Physiology, University of Johannesburg, Doornfontein, Johannesburg, South Africa,

autor

Mazengenya P.

• School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa

autor

Ihunwo A.O.

• School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa

Bibliografia

• Alunni A, Bally-Cuif L (2016) A comparative view of regenerative neurogenesis in vertebrates. Development 143: 741–753.
• Alvarez-Buylla A, Theelen M, Nottebohm F (1990) Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron 5: 101–109.
• Alvarez-Buylla A, Ling CY, Nottebohm F (1992) High vocal center growth and its relation to neurogenesis, neuronal replacement and song acquisition in juvenile canaries. J Neurobiol 23: 396–406.
• Alvarez-Buylla A, Ling CY, Yu WS (1994) Contribution of neurons born during embryonic and adult life to the brain of adult canaries: Regional specificity and delayed birth of neurons in the song-control nuclei. J Comp Neurol 347: 233–248.
• Balthazart J, Boseret G, Konkle A, Hurley lL, Ball GF (2008) Doublecortin as a marker of adult neuroplasticity in the canary song control nucleus HVC. Eur J Neurosci 27: 801–817.
• Balthazart J, Charlier TD, Barker JM, Yamamura T, Ball GF (2010) Sex steroid-induced neuroplasticity and behavioral activation in birds. Eur J Neurosci 32: 2116–2132.
• Balthazart J, Ball GF (2014a) Doublecortin is a highly valuable endogenous marker of adult neurogenesis in canaries. Brain Bev Evol 84: 1–4.
• Balthazart J, Ball GF (2014b) Endogenous versus exogenous markers of adult neurogenesis in canaries and other birds: advantages and disadvantages. J Comp Neurol 522: 4100–4120.
• Balthazart J, Ball GF (2016) Endocrine and social regulation of adult neurogenesis in songbirds. Front Neuroendocrinol 41: 3–22.
• Bardet SM, Mouriec K, Balthazart J (2012) Birth of neural progenitors during the embryonic period of sexual differentiation in the Japanese quail brain. J Comp Neurol 520: 4226–4253.
• Barker JM, Ball GF, Balthazart J (2014) Anatomically discrete sex differences and enhancement by testosterone of cell proliferation in the telencephalic ventricle zone of the adult canary brain. J Chem Neuroanat 55: 1–8.
• Barnea A, Pravosudov V (2011) Birds as a model to study adult neurogenesis: bridging evolutionary, comparative and neuroethological approaches. Eur J Neurosci 34: 884–907.
• Baylé J, Jamade F, Oliver J (1974) Stereotaxic topography of the brain of the quail (Coturnix coturnix japonica). J Physiol 68: 219–241.
• Boseret G, Ball GF, Balthazart J (2007) The microtubule-associated protein doublecortin is broadly expressed in the telencephalon of adult canaries. J Chem Neuroanat 33: 140–154.
• Brenowitz EA (2004) Plasticity of the adult avian song control system. Ann N Acad Sci 1016: 560–585.
• Brenowitz EA, Larson TA (2015) Neurogenesis in the adult avian song-control system. Cold Spring Harb Persepct Biol 7: a019000.
• Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner l, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467: 1–10.
• Capes-Davis A, Tolhurst O, Dunn JM, Jeffrey PL (2005) Expression of doublecortin (DCX) and doublecortin-like kinase (DCLK) within the developing chick brain. Dev Dyn 232: 457–467.
• Castagna C, Viglietti-Panzica C, Panzica GC (2003) Protein S100 immunoreactivity in glial cells and neurons of the Japanese quail brain. J Chem Neuroanat 25: 195–212.
• Charvet CJ, Striedter GF (2008) Developmental species differences in brain cell cycle rates between northern bobwhite quail (Colinus virginianus) and parakeets (Melopsittacus undulatus): implications for mosaic brain evolution. Brain Behav Evol 72: 295–306.
• DeWulf V, Bottjer SW (2002) Age and sex differences in mitotic activity within the zebra finch telencephalon. J Neurosci 22: 4080–4094.
• Essers J, Theil AF, Baldeyron C, Van Cappellen WA, Houtsmuller AB, Kanaar R, Vermeulen W (2005) Nuclear dynamics of PCNA in DNA replication and repair. Mol Cell Biol 25: 9350–9359.
• Guigueno MF, Macdougall-Shackleton SA, Sherry DF (2016) Sex and seasonal differences in hippocampal volume and neurogenesis in brood-parasitic brown-headed cowbirds (Molothrus ater). Dev Neurobiol 76: 1226–1240.
• Hall ZJ, Bauchinger U, Gerson AR, Price ER, Langlois IA, Boyles M, Pierce B, Mcwilliams SR, Sherry DF, Macdougall-Shackleton SA (2014) Site-specific regulation of adult neurogenesis by dietary fatty acid content, vitamin E and flight exercise in European starlings. Eur J Neurosci 39: 875–882.
• Horesh D, Sapir T, Francis F, Wolf SG, Caspi M, Elbaum M, Chelly J, Reiner O (1999) Doublecortin, a stabilizer of microtubules. Hum Mol Genet 8: 1599–1610.
• Kaslin J, Ganz J, Brand M (2008) Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans R Soc Lond B Biol Sci 363: 101–122.
• Klempin F, Kronenberg G, Cheung G, Kettenmann H, Kempermann G (2011) Properties of doublecortin-(DCX)-expressing cells in the piriform cortex compared to the neurogenic dentate gyrus of adult mice. PloS One 6: e25760.
• Kremer T, Jagasia R, Herrmann A, Matile H, Borroni E, Francis F, Kuhn HG, Czech C (2013) Analysis of adult neurogenesis: evidence for a prominent “non-neurogenic” DCX-protein pool in rodent brain. PloS One 8: e59269.
• Kuenzel WJ, Masson M (1988) A stereotaxic atlas of the brain of the chick (Gallus domesticus). Johns Hopkins University Press, Maryland, USA.
• Ling C, Cheng MF (1995) Sex differences in cell proliferation in the ventricular zone of young ring doves. Brain Res Bull 37: 657–662.
• Ling C, Zuo M, Alvarez-Buylla A, Cheng MF (1997) Neurogenesis in juvenile and adult ring doves. J Comp Neurol 379: 300–312.
• Maheu ME, Devorak J, Freibauer A, Davoli MA, Turecki G, Mechawar N (2015) Increased doublecortin (DCX) expression and incidence of DCX-immunoreactive multipolar cells in the subventricular zone-olfactory bulb system of suicides. Front Neuroanat 9: 74.
• Melleu F, Pinheiro M, Lino-De-Oliveira C, Marino-Neto J (2016) Defensive behaviors and prosencephalic neurogenesis in pigeons (Columba livia) are affected by environmental enrichment in adulthood. Brain Struct Funct 221: 2287–2301.
• Melleu F, Santos T, Lino-De-Oliveira C, Marino-Neto J (2013) Distribution and characterization of doublecortin-expressing cells and fibers in the brain of the adult pigeon (Columba livia). J Chem Neuroanat 47: 57–70.
• Meskenaite V, Krackow S, Lipp H-P (2016) Age-Dependent Neurogenesis and Neuron Numbers within the Olfactory Bulb and Hippocampus of Homing Pigeons. Front Behav Neurosci 10: 126.
• Mezey S, Krivokuca D, Bálint E, Adorján A, Zachar G, Csillag A (2012) Postnatal changes in the distribution and density of neuronal nuclei and doublecortin antigens in domestic chicks (Gallus domesticus). J Comp Neurol 520: 100–116.
• Mills AD, Crawford IL, Domjan M, Faure JM (1997) The behavior of the Japanese or domestic quail Coturnix japonica. Neurosci Biobehav Rev 21: 261–281.
• Mouriec K, Balthazart J (2013) Peripubertal proliferation of progenitor cells in the preoptic area of Japanese quail (Coturnix japonica). Brain Res 1516: 20–32.
• Nacher J, Crespo C, Mcewen BS (2001) Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14: 629–644.
• Nikolakopoulou A, Dermon C, Panagis l, Pavlidis M, Stewart M (2006a) Passive avoidance training is correlated with decreased cell proliferation in the chick hippocampus. Eur J Neurosci 24: 2631–2642.
• Nikolakopoulou A, Parpas A, Panagis l, Zikopoulos B, Dermon C (2006b) Early post-hatching sex differences in cell proliferation and survival in the quail telencephalic ventricular zone and intermediate medial mesopallium. Brain Res Bull 70: 107–116.
• Nottebohm F (1984) Birdsong as a model in which to study brain processes related to learning. Condor 86: 227–236.
• Nottebohm F (2011) Song learning in birds offers a model for neuronal replacement in adult brain. In: Neurogenesis in the Adult Brain I. Springer, Japan, p. 47–84.
• Olaleye OO, Ihunwo AO (2014) Adult neurogenesis in the four-striped mouse (Rhabdomys pumilio). Neural Regen Res 9: 1907–1911.
• Puelles L (2007) Chick brain in stereotaxic coordinates, Academic Press, San Diego, USA.
• Pytte CL, Gerson M, Miller J, Kirn JR (2007) Increasing stereotypy in adult zebra finch song correlates with a declining rate of adult neurogenesis. Dev Neurobiol 67: 1699–1720.
• Reiner A, Perkel DJ, Bruce IL, Butler AB, Csillag A, Kuenzel W, Medina I, Paxinos G, Shimizu T, Striedter G (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473: 377–414.
• Stamatakis A, Barbas H, Dermon C (2004) Late granule cell genesis in quail cerebellum. J Comp Neurol 474: 173–189.
• Striedter GF, Charvet CJ (2008) Developmental origins of species differences in telencephalon and tectum size: morphometric comparisons between a parakeet (Melopsittacus undulatus) and a quail (Colinus virgianus). J Comp Neurol 507: 1663–1675.
• Tsai HM, Garber BB, Larramendi lM (1981) 3H-Thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo: I. Neuronal birthdates of telencephalic compartments in situ. J Comp Neurol 198: 275–292.
• Vellema M, Van der Linden A, Gahr M (2010) Area-specific migration and recruitment of new neurons in the adult songbird brain. J Comp Neurol 518: 1442–1459.
• Wang N, Hurley P, Pytte C, Kirn IR (2002) Vocal control neuron incorporation decreases with age in the adult zebra finch. J Neurosci 22: 10864–10870.
• Yamamura T, Barker JM, Balthazart J, Ball GF (2011) Androgens and estrogens synergistically regulate the expression of doublecortin and enhance neuronal recruitment in the song system of adult female canaries. J Neurosci 31: 9649–9657.

Identyfikatory

DOI

10.21307/ane‑2018‑016