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Second-order sensory neurons are dependent on afferents from the sense organs during a critical period in development for their survival and differentiation. Past research has mostly focused on whole populations of neurons, hampering progress in understanding the mechanisms underlying these critical phases. To move toward a better understanding of the molecular and cellular basis of afferent-dependent neuronal development, we developed a new model to study the effects of ear removal on a single identifiable cell in the hindbrain of a frog, the Mauthner cell. Ear extirpation at various stages of Xenopus laevis development defines a critical period of progressively-reduced dependency of Mauthner cell survival/differentiation on the ear afferents. Furthermore, ear removal results in a progressively decreased reduction in the number of dendritic branches. Conversely, addition of an ear results in an increase in the number of dendritic branches. These results suggest that the duration of innervation and the number of inner ear afferents play a quantitative role in Mauthner cell survival/differentiation, including dendritic development.
Figure 1. Success of ear removal. (a) Percentage of animals with any form of ear regrowth at each stage of ear removal. (b) Control X. laevis at Stage 46. (c) Embryo in which the right ear was removed and replaced. (d) Embryo in which the right ear was removed. (dâ²) Immunohistochemistry for acetylated tubulin showing cranial nerves (roman numerals) and myoVI showing the absence of the ear on the right side as indicated by the absence of hair cells. (e) Embryo in which an additional ear was added rostral to the native right ear. (eâ²) Lipophilic dye labeling showing sensory neuron projections from both the native (red) and transplanted (green) ears into the vestibular nucleus in the hindbrain. Native ears are circled in black and labeled, Ear. Transplanted ear is circled in white. Scale bar is 0.5 mm in bâd and f; 200 µm in e; 25 µm in g.
Figure 2. Mauthner cell survival. (a) Dextran amine dye-labeled Mauthner cells in a control animal. (b) Dextran amine dye-labeled Mauthner cells in an animal in which the right ear was removed and immediately replaced. (c) Percentage of Mauthner cells present on the right side at the different stages of ear removal. (d) Dextran amine dye-labeled and (dâ²) 3A10 antibody immunohistochemistry showing the absence of the ipsilateral Mauthner cell following the removal of the right ear at Stage 28. (dâ³) Merge of d and dâ². (e) Higher magnification image showing bilateral Mauthner cell axon crossing in a control animal. (f) Higher magnification image showing bilateral Mauthner cell axon crossing in an animal in which the ear was removed and immediately replaced. (g) Higher magnification image showing only unilateral Mauthner cell axon crossing in an animal in which the right ear was removed at Stage 27. M, Mauthner cell; arrowheads indicate the crossing of two Mauthner cell axons. Scale bar is 50 µm.
Figure 3. Dendritic development of Mauthner cells following ear manipulation. (a) Dextran amine dye labeling and (aâ²) 3A10 immunohistochemistry of a Mauthner cell (M) showing filling of dendrites by dextran amine dye. (aâ³) Merge of a and aâ². (b) 3D reconstruction of a pair of Mauthner cells from a control embryo. (c) 3D reconstruction of a pair of Mauthner cells in which the right ear was removed and immediately replaced show little difference in the number of dendritic branches between Mauthner cells. (d) 3D reconstruction of a pair of Mauthner cells from an animal in which the right ear was removed at Stage 26 show a reduction in dendritic branching in the ipsilateral Mauthner cell. (e) 3D reconstruction of a pair of Mauthner cells from an animal in which an additional ear was transplanted rostral to the native ear at Stage 26 show an increase in dendritic branching in the ipsilateral Mauthner cell. (f) Number of dendritic branches following ear removal or ear addition. Dark shaded bars are left (control) Mauthner cells, light shaded bars are right (treated) Mauthner cells. ***, pâ<â0.001. (g) Median differences between left and right Mauthner cells following ear removal or ear addition. **represent significant difference from control, pâ<â0.005. (h) Sholl Analysis of the Mauthner cells on the right (treated) side in f. The number of dendritic branch crossings were counted at 25 µm intervals. Scale bar is 50 µm. Error bars are standard errors of the means.
Figure 4. Comparison of Mauthner cell dendritic branching following ear manipulation. Overlay of three right Mauthner cells from a control animal (yellow), an animal in which the ear was removed (magenta), and an animal with an extra ear (green). The number of dendritic branches (indicated in parenthesis) for the three representative Mauthner cells is approximately equal to the mean number of dendritic branches for each group as revealed in Fig. 3.
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