Cell proliferation in the Rana catesbeiana auditory medulla over metamorphic development

Abstract

During metamorphic development, bullfrogs (Rana catesbeiana) undergo substantial morphological, anatomical, and physiological changes as the animals prepare for the transition from a fully-aquatic to a semi-terrestrial existence. Using BrdU incorporation and immunohistochemistry, we quantify changes in cell proliferation in two key auditory brainstem nuclei, the dorsolateral nucleus and the superior olivary nucleus, over the course of larval and early postmetamorphic development. From hatchling through early larval stages, numbers of proliferating cells increase in both nuclei, paralleling the overall increase in total numbers of cells available for labeling. Numbers of proliferating cells in the superior olivary nucleus decrease during the late larval and deaf periods, and significantly increase during metamorphic climax. Proliferating cells in the dorsolateral nucleus increase in number from hatchling to late larval stages, decrease during the deaf period, and increase during climax. In both nuclei, numbers of proliferating cells decrease during the postmetamorphic froglet stage, despite increases in the number of cells available for label. Newly generated cells express either glial- or neural-specific phenotypes beginning between 1 week and 1 month post-BrdU injection, respectively, while some new cells express gamma-aminobutyric acid within 2 days of mitosis. Our data show that these auditory nuclei dramatically up-regulate mitosis immediately prior to establishment of a transduction system based on atmospheric hearing.

Cell proliferation during the early compartmentalization of the Xenopus laevis inner ear

“…The limitation of the immersion method is that beyond a certain animal size (S47), immersion is not an effective means for BrdU delivery to the otic vesicle. In our experiments, the efficacy of BrdU administration by im'mersion was confirmed in all specimens in this study through the presence of BrdU-positive cells in the ventricular zone of the brain (Chapman et al, 2006).…”

“…Amphibians such as Xenopus offer an alternative model for unraveling mechanisms that promote regeneration in an organism that is well characterized genetically and developmentally (Nieuwkoop and Faber, 1967;Amaya, 2005). Furthermore, the increasing interest in the use of amphibians such as Xenopus to investigate cell proliferation during development of the olfactory bulb (Fritz et al, 1996), the spinal cord (Schlosser et al, 2002) and the auditory medulla (Chapman et al, 2006), will provide a foundation for comparative studies of the regenerative potential of amphibian neural and sensory tissue as compared with that of other vertebrates. Here we have demonstrated the spatial and temporal patterns that characterize cell proliferation in the developing X. laevis inner ear during the period leading to the initial compartmentalization of auditory and vestibular structures at S47, as well as the contribution of cells that had undergone terminal mitosis during earlier stages to the formation of the emerging S47 sensory epithelia.…”

Plasticity of Auditory Medullary-Midbrain Connectivity across Metamorphic Development in the Bullfrog, <i>Rana catesbeiana</i>

“…Chapman et al [2006] observed stage-specific changes in cell proliferation in both the DMN and the SON, with peaks of cell birth in the early (DMN, SON) or late (DMN) larval periods, a decline during the deaf period, and a subsequent peak in metamorphic climax. Similarly, Templin and Simmons [2005] observed a decline in the number of differentiated neurons in the SON beginning during the deaf period and extending into the early stages of metamorphic climax.…”

“…Boundaries in the adult brain are based on Matesz [1979], Wilczynski [1981], Montgomery [1988], Will and Fritzsch [1988], Feng and Lin [1991], McCormick [1999] and Matesz et al [2002]. The DMN has been variously called the nucleus cochlearis [Larsell, 1934;Matesz, 1979], the acoustic nucleus [Jacoby and Rubinson, 1983] and the dorsal lateral nucleus Chapman et al, 2006]. What we are identifying as the anterior lateral line nucleus Opdam et al [1976].…”

“…The amount of terminal (puncta) label was categorized similarly, but with the number of cell bodies around which clusters of terminals were found as the unit of measure. The use of an individual tissue section as the unit of categorization allowed us to directly compare label across developmental stages, despite the differences in numbers of sections through the brainstem across development [Templin and Simmons, 2005;Chapman et al, 2006;. Categorizing the amount of label was made by all 3 authors independently, and the tables reflect the most common result from all sections in particular developmental groups.…”