Zeng SJ et al. (2008), Neurogenic development of the auditory areas of...

XB-ART-37383

Dev Biol 2008 Apr 24;1206:44-60. doi: 10.1016/j.brainres.2008.01.101.

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Neurogenic development of the auditory areas of the midbrain and diencephalon in the Xenopus laevis and evolutionary implications.

Zeng SJ , Tian C , Zhang X , Zuo MX .

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To study whether the core-versus-shell pattern of neurogenesis occurred in the mesencephalic and diencephalic auditory areas of amniotes also appears in the amphibian, [(3)H]-thymidine was injected into tadpoles at serial developmental stages of Xenopus laevis. Towards the end of metamorphism, [(3)H]-thymidine labeling was examined and led to two main observations: 1) neuron generation in the principal nucleus (Tp) started at stage 50, and peaked at stage 53, whereas it began at stage 48.5, and peaked around stage 49 in the other two mesencephalic auditory areas, the laminar nucleus (Tl) and the magnocellular nucleus (Tmc). 2) Neuron generation appeared at stage 40, and peaked around stage 52 in the posterior thalamic nucleus (P) and the central thalamic nucleus (C). Our study revealed that, like the cores of mesencephalic auditory nuclei in amniotes, Tp showed differences from Tl and Tmc in the onset and the peak of neurogenesis. However, such differences did not occur in the P and C. Our neurogenetic data were consistent with anatomical and physiological reports indicating a clear distinction between the mesencephalic, but not the diencephalic auditory areas of the amphibian. Our data are helpful to get insights into the organization of auditory nuclei and its evolution in vertebrates.

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Species referenced: Xenopus laevis
Genes referenced: ocm3

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	Fig. 1. Schematic diagrams of mesencephalic and diencephalic auditory areas in X. laevis around the end of metamorphosis. Mesencephalic auditory nucleus, comprising the principal nucleus (Tp), the laminar nucleus (Tl) and the magnocellular nucleus (Tmc), is equally divided into four portions with about 200 μm interval by three saggital planes (A1, B1 and C1). Diencephalic auditory nucleus, comprising the posterior thalamic nucleus (P) and the central thalamic nucleus (C), is equally divided into five parts with about 200 μm interval by four coronal brain planes (A2, B2, C2 and D2). The locations of saggital (A1–C1) and coronal (A2–D2) planes in the brain are shown in the insert (rostral is to the right). These planes will be adopted in the following figures. Dorsal is up for A1–D2, and medial is left for A2-D2. Scale bar = 0.5 mm for A1-D2. For other abbreviations, see list.
	Fig. 2. Nissl-staining (A, C and E) and immunoreactivity for substance P (B and D) and parvalbumin (F) in three sagittal planes of the torus semicircularis (TS). The locations of A, C and E in the brain are shown in Fig. 1A1, B1 and C1, respectively. Although images A–F are not from the same animal, A, C and E are located in similar brain positions to B, D and F, respectively. Tp boundaries shown by Nissl-staining and SP or PV immunohistochemistry are approximately consistent. However, Tp is smaller in SP immunohistochemistry than it in Nissl-staining. Scale bar represents 200 μm for A–F. For abbreviations, see list.
	Fig. 3. [3H]-thymidine labeling in the laminar nucleus (Tl). A and B: Peak of [3H]-thymidine labeling in the ventral Tl at stage 49 (A) and in the dorsal Tl at stage 51 (B) at the lateral brain plane (shown in Fig. 1A1). C–F: Peak of [3H]-thymidine labeling in the ventral Tl at stage 49 (C and D) and in the dorsal Tl at stage 53 (E and F) at the intermedial brain plane (shown in Fig. 1B1). G and H: Peak of [3H]-thymidine labeling in the ventral and dorsal Tl at stage 54 (B) at the medial brain plane (shown in Fig. 1C1). Dorsal and ventral portions are divided by dashed lines. D, F and H are the magnifications of the boxed areas in C, E and G, respectively. Some labeled cells are pointed by arrow heads. [3H]-thymidine labeling shows lateral (earlier, stage 49)-to-medial (later, stage 54) and dorsal-to-ventral neurogenetic gradients in lateral and intermedial sagittal planes (A–F), but not in the medial plane (G and H). Scale bar represents 50 μm for D, F and H, and 80 μm for others.
	Fig. 4. Percentages of labeled neurons during development in the laminar nucleus (Tl) and the magnocellular nucleus (Tmc). A–C: Percentages of labeled neurons in the dorsal and ventral portions of Tl at the A1 (A), B1 (B) and C1 (C) brain planes. A1–C1 planes are indicated in Fig. 1. D: Percentages of labeled neurons in the whole Tl (dorsal and ventral portions are combined) at A1–C1 brain planes. E: Percentages of labeled neurons in the dorsal and ventral Tmc, and in the whole Tmc (dorsal and ventral portions are combined). V: ventral portion. D: dorsal portion.
	Fig. 5. [3H]-thymidine labeling in the magnocellular nucleus (Tmc) and principal nucleus (Tp). A and B: Peak of [3H]-thymidine labeling in the ventral Tmc at stage 49 (A) and dorsal Tmc at stage 51 (B) at the lateral brain plane (shown in Fig. 1A1). C and D: [3H]-thymidine labeling first occurs only in the ventral Tp at stage 50 (C) and 51 (D) at the intermedial brain plane (shown in Fig. 1B1). E–H: Peak of [3H]-thymidine labeling in Tp at stage 53 at the intermedial brain plane (E and F), and at stage 54 at the medial brain plane (G and H). Dorsal and ventral portions were divided by dashed lines in A and B. F and H are the magnifications of the boxed areas in E and G, respectively. Some labeled cells are pointed by arrow heads. Scale bar represents 50 μm for A, B, F and H, and 80 μm for others.
	Fig. 6. Percentages of labeled neurons during development in the principal nucleus (Tp). A–D: Percentages of labeled neurons in the dorsal and ventral portions of Tp at the B1 (A), and C1 (C) brain planes, and in the rostral and caudal portions of Tp at the B1 (B), and C1 (D) brain planes. E: Percentages of labeled neurons in the whole Tp (dorsal/ventral and rostral/caudal portions are combined) at B1 and C1 brain planes. V: ventral. D: dorsal. R: rostral. C: caudal. B1 and C1: sagittal planes shown in Fig. 1.
	Fig. 7. Nissl-staining (A, C and E) and immunoreactivity for substance P (D1 and D2) and parvalbumin (B, F1 and F2) in three coronal planes of the diencephalic auditory areas. The location of A, C and E in the brain are shown in Fig. 1A2, C2 and D2, respectively. The brain locations are similar between A and B, and among D1/D2, F1/F2 and C. The insert of B is corresponded to the boxed area in A and B, and D2 corresponds to the boxed area in C and D1. F2 is the boxed area of F1. Some heavily labeled cells are pointed by arrow heads in B, F1 and F2. Scale bar represents 100 μm for the insert of B, D2 and F2, and 200 μm for others. For abbreviations, see list.
	Fig. 8. Percentages of labeled neurons during embryonic development in the posterior thalamic nucleus (P) and the central thalamic nucleus (C). A–C: Percentages of labeled neurons in the lateral and medial portions of P at the A2 (A), B2 (B) and C2 (C) brain planes. D: Percentages of labeled neurons in the whole P (lateral and medial portions are combined) at A2, B2 and C2 brain planes. E: Percentages of labeled neurons in the lateral and medial portions of C at the D2 brain plane. F: Percentages of labeled neurons in the whole P at B2, C2 and D2 brain planes. L: lateral. M: medial. R: rostral. C: caudal. A2, B2, C2 and D2: sagittal planes shown in Fig. 1.
	Fig. 9. [3H]-thymidine labeling in the posterior (P) (A–L), and the central thalamic nucleus (C) (M–P) at the four coronal planes (corresponding to A2–D2 planes in Fig. 1). A and B: [3H]-thymidine in the lateral P first occurs in the caudal plane at stage 40 (A), and in the caudomedial plane at stage 51 (B). C–F: Peak of [3H]-thymidine labeling in the lateral P at stage 47 (C and D), and in the medial P at stage 54 (E and F) at the caudal brain plane. G–J: Peak of [3H]-thymidine labeling in the lateral P at stage 50 (G and H), and in the medial P at stage 54 (I and J) at the caudomedial brain plane. K and L: Peak of [3H]-thymidine labeling in P at stage 54 at the rostromedial brain plane. M–O: Peak of [3H]-thymidine labeling in the lateral C at stage 50 (M and N), and in the rostromedial plane in C at stage 51 (O) at the rostral brain plane. P: Peak of [3H]-thymidine labeling in the medial C at stage 54 at the rostral brain plane. Lateral and medial portions were divided by dashed lines. D, F, H, L, M and P are the magnifications of the boxed areas in C, E, G, K, M and O, respectively. Some labeled cells are pointed by arrow heads. Scale bar represents 50 μm for D, F, H, J, L and N, and 80 μm for others.
	Fig. 10. Cells labeled by [3H]-thymidine and the pre-neuronal marker Hu. A-B: Labeled cells in the laminar nucleus (Tl) and the principal nucleus (Tp) at the stage 54 (A) and 55 (B). The locations of A and B in the brain are corresponded to Fig. 1 ; Fig. 2 C or D, respectively. C–E: Labeled cells in the posterior thalamic nucleus (P) and the central thalamic nucleus (C) at the stage 56. The locations of C, D and E in the brain are corresponded to Fig. 1 B2, D2 and C2, respectively. F: Labeled cells in the Tp at the stage 56. Some double-labeled cells are pointed by arrowheads. Some labeled cells only by [3H]-thymidine are marked with asterisk, and these cells are rich in the thalamic ventricle (C-E). Scale bar represents 50 μm from A to E.