Sex difference in cellular proliferation within the telencephalic ventricle zone of Bengalese finch☆
Introduction
Sexual differentiation in song behavior is reflected by high sexual dimorphism of song control nuclei. Male song control nuclei are larger in volume (Nottebohm and Arnold, 1976), cell size, and cell number relative to those of females (Gurney, 1981, Nordeen et al., 1987). Sexual differentiation of song nuclei is produced in two ways. (1) HVC and Area X, whose neurons are largely born during the first 20 days post-hatching (Alvarez-Buylla and Nottebohm, 1988), exhibit sex differences as a result of large increases in cellular numbers in males, but not in females (Nordeen and Nordeen, 1988; Burek et al., 1995, Burek et al., 1997; Kim et al., 2004, Wade and Arnold, 2004). (2) Other song control nuclei, such as the robust nucleus of the arcopallium (RA) and lateral magnocellular nucleus of anterior nidopallium (LMAN), exhibit sexual dimorphism after neurons have finished migration and initial differentiation, resulting in neuronal growth in males and neuronal shrinkage or death in females (Alvarez-Buylla and Nottebohm, 1988, Konish and Akutagawa, 1990, Alvarez-Buylla et al., 1994; Burek et al., 1994, Burek et al., 1995). Female birds can be masculinized by administration of estradiol early in development or during the critical period of development (Konishi and Akutagawa, 1985, Konish and Akutagawa, 1988, Nordeen and Nordeen, 1989).
Cell survival, migration and specification are known to contribute to sex differences in the net addition of song control nuclei neurons (Goldman and Nottebohm, 1983, Nordeen and Nordeen, 1988, Kirn et al., 1994). However, cellular proliferation within the ventricular zone (VZ), which is another potential mechanism underlying sexual differentiation in song control nuclei such as HVC and Area X, has not been studied in detail (DeWulf and Bottjer, 2002, DeWulf and Bottjer, 2005). To address this issue we administered [3H]thymidine to juvenile bengalese finches (Lonchura striata) of both sexes 15 days post-hatching, within the critical period of sexual differentiation of the song control system. The birds were killed 2 h later to examine proliferation activity uncombined with cell death or migration away from the VZ. In addition, to further disclose the potential role that estradiol may play in cell proliferation within the VZ, we compared cellular proliferation between females implanted with estradiol benzoate (EB) at age of 5 days post-hatching and those receiving empty implants.
Section snippets
Thymidine labeling and tissue preparation
Fifty-five Bengalese finches were taken from our breeding colony to measure levels of cellular proliferation in VZ. Of these, twelve birds received a 3 mm subcutaneous Silastic implant filled with EB (75 μg, Sigma), while twelve birds received an empty Silastic implant. Each bird then received a single intramuscular injection of [3H]thymidine (2.5 μCi/g dose; specific activity, 6.7 Ci/mmol; New England Nuclear) at 15 days of age. All individuals were killed 2 h later. Two hours survival is short
Cellular proliferation at the brain level of HVC
Clusters of thymidine labeled cells were observed within the VZ (Fig. 2). Although scattered clusters of thymidine labeling were distributed along the entire extent of the VZ, and not localized to a specific region (Fig. 1c), a greater number of labeled cells appeared at the dorsal VZ. Because labeled cells did not overlap (Fig. 2), we could count labeled cells individually.
There was a significant trend toward decreased number of thymidine labeled cells along the seven dorsal–ventral bins in
Discussion
Since new HVC and Area X neurons require 1–3 weeks to arrive in song-control nuclei after they are produced within the VZ (Burd and Nottebohm, 1985, Alvarez-Buylla and Nottebohm, 1988, Burek et al., 1994, Kirn et al., 1999), such long post-generation intervals may cause varied numbers of neurons in targeted regions, due to subsequent cell division, differentiation, cell death and migration (Alvarez-Buylla and Nottebohm, 1988, Konish and Akutagawa, 1990; Burek et al., 1994, Burek et al., 1995).
References (60)
Tactile contact is required for early estrogen treatment to alter the sexual partner preference of female zebra finches
Horm. Behav.
(2005)- et al.
Sex steroids modulate changes in social and sexual preference during juvenile development in zebra finches
Horm. Behav.
(2006) - et al.
Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division
Neuron
(1990) - et al.
Ontogeny of sex differences among newly-generated neurons of the juvenile avian brain
Brain Res. Dev. Brain Res.
(1994) - et al.
Estrogen promotes neuron addition to an avian song-control nucleus by regulating post-mitotic events.
Brain Res. Dev. Brain Res.
(1995) A neural circuit specialized for vocal learning
Curr. Opin. Neurobiol.
(1993)- et al.
Brain bFGF stimulates the proliferation of rat neuronal precursor cells in vitro
FEBS Lett.
(1987) - et al.
Sex differences in cell proliferation in the ventricular zone of young ring doves
Brain Res. Bull.
(1995) - et al.
Early post-hatching sex differences in cell proliferation and survival in the quail telencephalic ventricular zone and intermediate medial mesopallium
Brain Res. Bull.
(2006) - et al.
Estrogen stimulates the incorporation of new neurons into avian song nuclei during adolescence
Brain Res. Dev. Brain Res.
(1989)
Song syntax in Bengalese finches:proximate and ultimate analyses
Adv. Study Behav.
Activities of 3beta-HSD and aromatase in slices of developing and adult zebra finch brain
Gen. Comp. Endocrinol.
Migration of young neurons in adult avian brain
Nature
Contribution of neurons born during embryonic, juvenile, and adult life to the brain of adult canaries: regional specificity and delayed birth of neurons in the song control nuclei
J. Comp. Neurol.
Birth, migration, incorporation, and death of vocal control neurons in adult songbirds
J. Neurobiol.
Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes
Science
Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria)
J. Neurobiol.
Neurogenesis in adult canary telencephalon is independent of gonadal hormone levels
J. Neurosci.
Ultrastructural characterization of synapticterminals formed on newly generated neurons in a song control nucleus of the adult canary forebrain
J. Comp. Neurol.
Sexually dimorphic neuron addition to an avian song-control region is not accounted for by sex differences in cell death
J. Neurobiol.
Glial cell lineage in the cerebral cortex: a review and synthesis
Glia
Age and sex differences in mitotic activity within the zebra finch telencephalon
J. Neurosci.
Neurogenesis within the juvenile zebra finch telencephalic ventricular zone: a map of proliferative activity
J. Comp. Neurol.
Estrogen-inducible, sex-specific expression of brain-derived neurotrophic factor mRNA in a forebrain song control nucleus of the juvenile zebra finch
Proc. Natl. Acad. Sci. U.S.A.
The development of chick spinal cord in tissue culture: neuronal precursor cells in culture
In vitro
Dispersion of neural progenitors within the germinal zones of the forebrain
Nature
Developmental changes in esdrogen-sensitive neurons in the forebrain of the zebra finch
Proc. Natl. Acad. Sci. U.S.A.
Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain
Proc. Natl. Acad. Sci. U.S.A.
Migration of newly generated neurons upon ependymally-derived radial guide cells in explant cultures of the adult avian forebrain
Glia
Ependymal/subependymal zone cells of postnatal and adult songbird brain generate both neurons and nonneuronal siblings in vitro and in vivo
J. Neurobiol.
Cited by (11)
Neuroestradiol and neuronal development: Not an exclusive male tale anymore
2023, Frontiers in NeuroendocrinologyNotch1 is involved in cell proliferation and neuronal differentiation in the HVC of zebra finch (Taeniopygia guttata)
2023, Behavioural Brain ResearchAnatomically discrete sex differences and enhancement by testosterone of cell proliferation in the telencephalic ventricle zone of the adult canary brain
2014, Journal of Chemical NeuroanatomyCitation Excerpt :However, sex differences in proliferation have been reported in juvenile zebra finches in anatomically discrete brain regions, confined to the ventral and rostral part of the VZ at the level of Area X (DeWulf and Bottjer, 2002, 2005). Studies of 15-day-old Bengalese finches also revealed localized sex differences in cell proliferation that the authors related to the development of sex differences in the morphology of the song nuclei HVC and Area X (Zeng et al., 2007). Because adult females are often used to investigate cellular effects of testosterone on adult plasticity in songbirds, it is useful to confirm that cells in both sexes respond similarly to the steroid.
Identification of male-biased gene: Parvalbumin in song control nuclei of the Bengalese finch
2010, Neuroscience ResearchSexual differentiation of brain and behavior in birds
2009, Hormones, Brain and Behavior Online
- ☆
Grant sponsor: National Natural Science Foundation of China to SJ Zeng (No.: 30470226), MX Zuo (No.: 30670685) and XW Zhang (No.: 30460042), and Beijing Natural Science Foundation of China to MX Zuo (No. 5052016).