Cellular and spatial changes in the anuran superior olive across metamorphosis

Templin, Thomas; Simmons, Andrea Megela

doi:10.1016/j.heares.2005.04.006

Cited by 9 publications

(19 citation statements)

References 45 publications

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“…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. Numbers of neurons then increase during the later stages of metamorphic climax and the froglet period.…”

Section: Possible Mechanisms Of Anatomical Reorganizationmentioning

confidence: 77%

“…This suggests that younger tissue may simply not label or process as well as more mature tissue, perhaps due to differences in extent of dendritic arborizations. At least in the SON, soma size does not consistently increase across larval development [Templin and Simmons, 2005].…”

Section: Technical Considerationsmentioning

confidence: 95%

“…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.…”

Section: Image Processing and Analysesmentioning

confidence: 99%

“…In Rana and other frogs that do not remain totally aquatic after metamorphosis, this change in position occurs concomitantly with the degeneration of the lateral line neuropil and lateral line nuclei [Larsell, 1934;Fritzsch et al, 1984Fritzsch et al, , 1988. In contrast, the superior olivary nucleus (SON) does not appear to migrate in position but it does vary considerably in cell density and nuclear volume over larval development [Templin and Simmons, 2005]. Three major subdivisions of the midbrain torus semicircularis (TS) that are apparent in adult frogs [Feng and Lin, 1991] are largely undifferen- tiated in tadpoles, and it is not until metamorphic climax and the froglet period that these divisions become morphologically distinct [Boatright-Horowitz and Simmons, 1995;Kumaresan et al, 1998].…”

Section: Introductionmentioning

confidence: 99%

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

Horowitz¹,

Chapman²,

Simmons³

2006

Brain Behav Evol

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On the basis of patterns of anterograde, retrograde, and bi-directional transport of tracers from both the superior olivary nucleus (SON) and the torus semicircularis (TS), we report anatomical changes in brainstem connectivity across metamorphic development in the bullfrog, Rana catesbeiana. In early and late stages of larval development (Gosner stages 25–37), anterograde or bi-directional tracers injected into the SON produce terminal/fiber label in the contralateral SON and in the ipsilateral TS. Between stages 38–41 (deaf period), only sparse or no terminal/fiber label is visible in these target nuclei. During metamorphic climax (stages 42–46), terminal/fiber label reappears in both the contralateral SON and in the ipsilateral TS, and now also in the contralateral TS. Injections of retrograde tracers into the SON fail to label cell bodies in the ipsilateral TS in deaf period animals, mirroring the previously-reported failure of retrograde transport from the TS to the ipsilateral SON during this developmental time. Bilateral cell body label emerges in the dorsal medullary nucleus and the lateral vestibular nucleus bilaterally as a result of SON transport during the late larval period, while cell body label in the contralateral TS emerges during climax. At all larval stages, injections into the SON produce anterograde and retrograde label in the medial vestibular nucleus bilaterally. These data show anatomical stability in some pathways and plasticity in others during larval development, with the most dramatic changes occurring during the deaf period and metamorphic climax. Animals in metamorphic climax show patterns of connectivity similar to that of froglets and adults, indicating the maturation during climax of central anatomical substrates for hearing in air.

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Section: Possible Mechanisms Of Anatomical Reorganizationmentioning

confidence: 77%

Section: Technical Considerationsmentioning

confidence: 95%

Section: Image Processing and Analysesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Horowitz¹,

Chapman²,

Simmons³

2006

Brain Behav Evol

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“…Although some of these changes have been previously reported (Jacoby and Rubinson, 1983;Templin and Simmons, 2005), they are highlighted in the medullary morph video (Online supplemental materials, MedullaCVmorph.avi). Moreover, the video shows developmental trends in other medullary areas that have not been previously described.…”

Section: Resultsmentioning

confidence: 95%

Dynamic visualization of the developing nervous system of the bullfrog, Rana catesbeiana

Horowitz

Simmons

2007

Brain Research

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Anuran amphibians undergo a rapid and dramatic process of metamorphosis featuring widespread structural reorganization of the central nervous system. Although morphological changes during embryonic stages of anuran development have been well-documented, much less information is available describing structural changes in the brain during larval (tadpole) stages. Using still images from cresyl violet stained material, we present an adaptation of the digital image and video manipulation technique of morphing that allows these images to be compiled in such a manner as to highlight key periods in tadpole brain development in a dynamic fashion. We present three morphed video data sets from ranid tadpoles that facilitate the identification of developmental changes in nuclear boundaries at different levels of the neuraxis. The use of animation allows dynamic examination of anatomical changes across long developmental spans without requiring additional anatomical preparations or specialized expensive equipment. Section: Structural Organization of the Brain

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Cell proliferation in the Rana catesbeiana auditory medulla over metamorphic development

2005

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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.

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Cellular and spatial changes in the anuran superior olive across metamorphosis

Cited by 9 publications

References 45 publications

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

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

Dynamic visualization of the developing nervous system of the bullfrog, Rana catesbeiana

Cell proliferation in the Rana catesbeiana auditory medulla over metamorphic development

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