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Sexual Differences in Cell Loss during the Post-Hatch Development of Song Control Nuclei in the Bengalese Finch.

Chen X, Li J, Zeng L, Zhang X, Lu X, Zuo M, Zhang X, Zeng S - PLoS ONE (2015)

Bottom Line: A corresponding sharp decrease in the density of Bcl-2 after P35 was observed in both sexes, and a greater density of Bid was noted at P45 in males.In addition, we observed that RA volume and the total number of BDNF-expressing cells decreased significantly after unilateral lesion of the LMAN or HVC (two areas that innervate the RA) and that greater numbers of RA-projecting cells were immunoreactive for BDNF in the LMAN than in the HVC.We reasoned that a decrease in the amount of BDNF transported via HVC afferent fibers might result in an increase in cell apoptosis in the female RA.

View Article: PubMed Central - PubMed

Affiliation: Beijing Key Laboratory of Gene Resource and Molecular Development, Beijing Normal University, Beijing, China.

ABSTRACT
Birdsongs and the regions of their brain that control song exhibit obvious sexual differences. However, the mechanisms underlying these sexual dimorphisms remain unknown. To address this issue, we first examined apoptotic cells labeled with caspase-3 or TUNEL in Bengalese finch song control nuclei - the robust nucleus of the archopallium (RA), the lateral magnocellular nucleus of the anterior nidopallium (LMAN), the high vocal center (HVC) and Area X from post-hatch day (P) 15 to 120. Next, we investigated the expression dynamics of pro-apoptotic (Bid, Bad and Bax) and anti-apoptotic (Bcl-2 and Bcl-xL) genes in the aforementioned nuclei. Our results revealed that the female RA at P45 exhibited marked cell apoptosis, confirmed by low densities of Bcl-xL and Bcl-2. Both the male and female LMAN exhibited apoptotic peaks at P35 and P45, respectively, and the observed cell loss was more extensive in males. A corresponding sharp decrease in the density of Bcl-2 after P35 was observed in both sexes, and a greater density of Bid was noted at P45 in males. In addition, we observed that RA volume and the total number of BDNF-expressing cells decreased significantly after unilateral lesion of the LMAN or HVC (two areas that innervate the RA) and that greater numbers of RA-projecting cells were immunoreactive for BDNF in the LMAN than in the HVC. We reasoned that a decrease in the amount of BDNF transported via HVC afferent fibers might result in an increase in cell apoptosis in the female RA. Our data indicate that cell apoptosis resulting from different pro- and anti-apoptotic agents is involved in generating the differences between male and female song control nuclei.

No MeSH data available.


Related in: MedlinePlus

Immunohistochemistry for TrkB in the RA, LMAN, HVC and Area X in the Bengalese finch.A1–D2: Labeled cells in the RA at post-hatching day (P) 15 (A1, A2), the LMAN at P25 (B1, B2), the HVC at P15 (C1, C2), and in Area X at P45 (D1, D2). E-H: Comparisons of the densities of TrkB-positive cells in the RA (E), LMAN (F), HVC (G) and Area X (H) between males and females. Borders of the song nuclei (dashed lines) were determined with the help of another set of Nissl-stained sections. The Nissl-defined border of the female Area X was difficult to clearly identify, and the dashed lines in D2 indicate the approximate region corresponding to the male Area X. Dorsal is up and caudal is right. Scale bar = 200 μm in A1–C2 and 300 μm in D1–D2. The data are expressed as the mean ± SEM. *P< 0.05, **P< 0.01.
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pone.0125802.g007: Immunohistochemistry for TrkB in the RA, LMAN, HVC and Area X in the Bengalese finch.A1–D2: Labeled cells in the RA at post-hatching day (P) 15 (A1, A2), the LMAN at P25 (B1, B2), the HVC at P15 (C1, C2), and in Area X at P45 (D1, D2). E-H: Comparisons of the densities of TrkB-positive cells in the RA (E), LMAN (F), HVC (G) and Area X (H) between males and females. Borders of the song nuclei (dashed lines) were determined with the help of another set of Nissl-stained sections. The Nissl-defined border of the female Area X was difficult to clearly identify, and the dashed lines in D2 indicate the approximate region corresponding to the male Area X. Dorsal is up and caudal is right. Scale bar = 200 μm in A1–C2 and 300 μm in D1–D2. The data are expressed as the mean ± SEM. *P< 0.05, **P< 0.01.

Mentions: We compared the distributions of BDNF- and TrkB-positive cells in the four studied song nuclei of both sexes (BDNF: Fig 6; TrkB: Fig 7). Our results indicated that the densities of BDNF- and TrkB-positive cells were significantly different across the five age groups in the RA (BDNF: F(4, 23) = 66.667, P<0.001, Fig 6A1, 6A2 and 6E; TrkB: F(4, 23) = 20.035, P<0.001, Fig 7A1, 7A2 and 7E), LMAN (BDNF: F(4, 23) = 13.763, P<0.001, Fig 6B1, 6B2 and 6F; TrkB: F(4, 23) = 20.603, P<0.001, Fig 7B1, 7B2 and 7F), HVC (BDNF: F(4, 23) = 7.662, P = 0.001, Fig 6C1, 6C2 and 6G) and Area X (BDNF: F(4, 23) = 20.328, P<0.001, Fig 6D1, 6D2 and 6H; TrkB: F(4, 23) = 7.603, P = 0.001, Fig 7D1, 7D2 and 7H). However, TrkB density did not differ in the HVC (TrkB: F(4, 23) = 1.325, P = 0.295, Fig 7C1, 7C2 and 7G). There were significant sexual differences in the density of BDNF-positive cells in the RA at P25 (t = -4.610, P = 0.001, n = 5, Fig 6A1, 6A2 and 6E) and in the adult (t = -11.156, P<0.001, n = 5, Fig 6E), in the HVC at P15 (t = 6.705, P = 0.003, n = 4, Fig 6C1, 6C2 and 6G), and in the Area X at P35 (t = 6.626, P = 0.003, n = 5, Fig 6D1, 6D2 and 6H) and P45 (t = 4.114, P = 0.015, n = 5, Fig 6H), but no differences were found in the LMAN (F(1, 23) = 0.788, P = 0.385, Fig 6B1, 6B2 and 6F). Similar to BDNF, there were significant sexual differences in the density of TrkB-positive cells in the RA at P15 (t = -3.700, P = 0.021, n = 5, Fig 7A1, 7A2 and 7E) and in the adult (t = -5.434, P = 0.006, n = 5, Fig 7E), in the HVC at P15 (t = 10.920, P<0.001, n = 4, Fig 7C1, 7C2 and 7G), P25 (t = 12.825, P<0.001, n = 5, Fig 7G) and P35 (t = 2.825, P = 0.048, n = 5, Fig 7G), and in the Area X at P45 (t = 3.708, P = 0.049, n = 5, Fig 7D1, 7D2 and 7H) and in the adult (t = 4.511, P = 0.011, n = 5, Fig 7H), but no differences were present in the LMAN for any of the studied age groups (F(1, 23) = 0.862, P = 0.346, Fig 7B1, 7B2 and 7F).


Sexual Differences in Cell Loss during the Post-Hatch Development of Song Control Nuclei in the Bengalese Finch.

Chen X, Li J, Zeng L, Zhang X, Lu X, Zuo M, Zhang X, Zeng S - PLoS ONE (2015)

Immunohistochemistry for TrkB in the RA, LMAN, HVC and Area X in the Bengalese finch.A1–D2: Labeled cells in the RA at post-hatching day (P) 15 (A1, A2), the LMAN at P25 (B1, B2), the HVC at P15 (C1, C2), and in Area X at P45 (D1, D2). E-H: Comparisons of the densities of TrkB-positive cells in the RA (E), LMAN (F), HVC (G) and Area X (H) between males and females. Borders of the song nuclei (dashed lines) were determined with the help of another set of Nissl-stained sections. The Nissl-defined border of the female Area X was difficult to clearly identify, and the dashed lines in D2 indicate the approximate region corresponding to the male Area X. Dorsal is up and caudal is right. Scale bar = 200 μm in A1–C2 and 300 μm in D1–D2. The data are expressed as the mean ± SEM. *P< 0.05, **P< 0.01.
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Related In: Results  -  Collection

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pone.0125802.g007: Immunohistochemistry for TrkB in the RA, LMAN, HVC and Area X in the Bengalese finch.A1–D2: Labeled cells in the RA at post-hatching day (P) 15 (A1, A2), the LMAN at P25 (B1, B2), the HVC at P15 (C1, C2), and in Area X at P45 (D1, D2). E-H: Comparisons of the densities of TrkB-positive cells in the RA (E), LMAN (F), HVC (G) and Area X (H) between males and females. Borders of the song nuclei (dashed lines) were determined with the help of another set of Nissl-stained sections. The Nissl-defined border of the female Area X was difficult to clearly identify, and the dashed lines in D2 indicate the approximate region corresponding to the male Area X. Dorsal is up and caudal is right. Scale bar = 200 μm in A1–C2 and 300 μm in D1–D2. The data are expressed as the mean ± SEM. *P< 0.05, **P< 0.01.
Mentions: We compared the distributions of BDNF- and TrkB-positive cells in the four studied song nuclei of both sexes (BDNF: Fig 6; TrkB: Fig 7). Our results indicated that the densities of BDNF- and TrkB-positive cells were significantly different across the five age groups in the RA (BDNF: F(4, 23) = 66.667, P<0.001, Fig 6A1, 6A2 and 6E; TrkB: F(4, 23) = 20.035, P<0.001, Fig 7A1, 7A2 and 7E), LMAN (BDNF: F(4, 23) = 13.763, P<0.001, Fig 6B1, 6B2 and 6F; TrkB: F(4, 23) = 20.603, P<0.001, Fig 7B1, 7B2 and 7F), HVC (BDNF: F(4, 23) = 7.662, P = 0.001, Fig 6C1, 6C2 and 6G) and Area X (BDNF: F(4, 23) = 20.328, P<0.001, Fig 6D1, 6D2 and 6H; TrkB: F(4, 23) = 7.603, P = 0.001, Fig 7D1, 7D2 and 7H). However, TrkB density did not differ in the HVC (TrkB: F(4, 23) = 1.325, P = 0.295, Fig 7C1, 7C2 and 7G). There were significant sexual differences in the density of BDNF-positive cells in the RA at P25 (t = -4.610, P = 0.001, n = 5, Fig 6A1, 6A2 and 6E) and in the adult (t = -11.156, P<0.001, n = 5, Fig 6E), in the HVC at P15 (t = 6.705, P = 0.003, n = 4, Fig 6C1, 6C2 and 6G), and in the Area X at P35 (t = 6.626, P = 0.003, n = 5, Fig 6D1, 6D2 and 6H) and P45 (t = 4.114, P = 0.015, n = 5, Fig 6H), but no differences were found in the LMAN (F(1, 23) = 0.788, P = 0.385, Fig 6B1, 6B2 and 6F). Similar to BDNF, there were significant sexual differences in the density of TrkB-positive cells in the RA at P15 (t = -3.700, P = 0.021, n = 5, Fig 7A1, 7A2 and 7E) and in the adult (t = -5.434, P = 0.006, n = 5, Fig 7E), in the HVC at P15 (t = 10.920, P<0.001, n = 4, Fig 7C1, 7C2 and 7G), P25 (t = 12.825, P<0.001, n = 5, Fig 7G) and P35 (t = 2.825, P = 0.048, n = 5, Fig 7G), and in the Area X at P45 (t = 3.708, P = 0.049, n = 5, Fig 7D1, 7D2 and 7H) and in the adult (t = 4.511, P = 0.011, n = 5, Fig 7H), but no differences were present in the LMAN for any of the studied age groups (F(1, 23) = 0.862, P = 0.346, Fig 7B1, 7B2 and 7F).

Bottom Line: A corresponding sharp decrease in the density of Bcl-2 after P35 was observed in both sexes, and a greater density of Bid was noted at P45 in males.In addition, we observed that RA volume and the total number of BDNF-expressing cells decreased significantly after unilateral lesion of the LMAN or HVC (two areas that innervate the RA) and that greater numbers of RA-projecting cells were immunoreactive for BDNF in the LMAN than in the HVC.We reasoned that a decrease in the amount of BDNF transported via HVC afferent fibers might result in an increase in cell apoptosis in the female RA.

View Article: PubMed Central - PubMed

Affiliation: Beijing Key Laboratory of Gene Resource and Molecular Development, Beijing Normal University, Beijing, China.

ABSTRACT
Birdsongs and the regions of their brain that control song exhibit obvious sexual differences. However, the mechanisms underlying these sexual dimorphisms remain unknown. To address this issue, we first examined apoptotic cells labeled with caspase-3 or TUNEL in Bengalese finch song control nuclei - the robust nucleus of the archopallium (RA), the lateral magnocellular nucleus of the anterior nidopallium (LMAN), the high vocal center (HVC) and Area X from post-hatch day (P) 15 to 120. Next, we investigated the expression dynamics of pro-apoptotic (Bid, Bad and Bax) and anti-apoptotic (Bcl-2 and Bcl-xL) genes in the aforementioned nuclei. Our results revealed that the female RA at P45 exhibited marked cell apoptosis, confirmed by low densities of Bcl-xL and Bcl-2. Both the male and female LMAN exhibited apoptotic peaks at P35 and P45, respectively, and the observed cell loss was more extensive in males. A corresponding sharp decrease in the density of Bcl-2 after P35 was observed in both sexes, and a greater density of Bid was noted at P45 in males. In addition, we observed that RA volume and the total number of BDNF-expressing cells decreased significantly after unilateral lesion of the LMAN or HVC (two areas that innervate the RA) and that greater numbers of RA-projecting cells were immunoreactive for BDNF in the LMAN than in the HVC. We reasoned that a decrease in the amount of BDNF transported via HVC afferent fibers might result in an increase in cell apoptosis in the female RA. Our data indicate that cell apoptosis resulting from different pro- and anti-apoptotic agents is involved in generating the differences between male and female song control nuclei.

No MeSH data available.


Related in: MedlinePlus