Developmental changes in cell proliferation in the auditory midbrain of the bullfrog, Rana catesbeiana

Simmons, Andrea Megela; Chapman, Judith; Brown, Rebecca

doi:10.1002/neu.20301

Cited by 10 publications

(14 citation statements)

References 46 publications

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“…In the rat cortex, this protein is expressed only transiently during development, and is 'almost undetectable' in the adult. In the bullfrog brainstem, TOAD-64 is also expressed during development Simmons et al, 2006], but, in contrast to the rat cortex, it remains detectable in adults [this study]. This continued presence of TOAD-64 label lends support to the contention that the adult bullfrog brain contains early postmitotic neurons.…”

Section: Discussionsupporting

confidence: 62%

“…These authors suggested that birth of new cells occurs in the striatum but that these cells do not survive. Simmons et al [2006] estimated the percentages of double-labeled cells in the TS of recently metamorphosed froglets surviving 30 days post-BrdU injection to be approximately 20% (BrdU-GFAP) and 10% (BrdU-TOAD-64). These estimates in the froglet TS are within the same general range as those obtained in the adult TS at a similar survival time [this study].…”

Section: Discussionmentioning

confidence: 99%

“…These animals show considerable cell birth in mesencephalic and rhombencephalic nuclei throughout the prolonged period of larval development and into the early postmetamorphic period Simmons et al, 2006]. There is only limited information on the extent of cell proliferation in the brains of any amphibian species during adulthood, even though adult amphibians show functional recovery after injury [Dieringer, 1995].…”

Section: Introductionmentioning

confidence: 99%

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Cell Proliferation in the Forebrain and Midbrain of the Adult Bullfrog, Rana catesbeiana

Simmons¹,

Horowitz²,

Brown

2007

Brain Behav Evol

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The distribution of proliferating cells in the midbrain, thalamus, and telencephalon of adult bullfrogs (Rana catesbeiana) was examined using immunohistochemistry for the thymidine analog 5-bromo-2′-deoxyuridine (BrdU) and DNA dot-blotting. At all time points examined (2 to 28 days post-injection), BrdU-labeled cells were located in ventricular zones at all levels of the neuraxis, but with relatively more label around the telencephalic ventricles. Labeled cells, some showing profiles indicative of dividing and migrating cells, were present in brain parenchyma from 7 to 28 days post-injection. These labeled cells were particularly numerous in the dorsal and ventral hypothalamus, preoptic area, optic tectum, and laminar and principal nuclei of the torus semicircularis, with label also present, but at qualitatively reduced levels, in thalamic and telencephalic nuclei. Double-label immunohistochemistry using glial and early neural markers indicated that gliogenesis and neurogenesis both occurred, with new neurons observed particularly in the hypothalamus, optic tectum, and torus semicircularis. In all brain areas, many cells not labeled with BrdU were nonetheless labeled with the early neural marker TOAD-64, indicating that these cells were postmitotic. Incorporation of DNA measured by dot-blotting confirms the presence of DNA synthesis in the forebrain and brainstem at all time points measured. The pattern of BrdU label confirms previous experiments based on labeling with ³H-thymidine and proliferating cell nuclear antigen showing cell proliferation in the adult ranid brain, particularly in hypothalamic nuclei. The consistent appearance of new cells in the hypothalamus of adult frogs suggests that proliferative activity may be important in mediating reproductive behaviors in these animals.

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Section: Discussionsupporting

confidence: 62%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Cell Proliferation in the Forebrain and Midbrain of the Adult Bullfrog, Rana catesbeiana

Simmons¹,

Horowitz²,

Brown

2007

Brain Behav Evol

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“…Consistent with these findings, our data show some parallels between GAP-43 immunoreactivity and periods of cell proliferation in both the SON and the TS. Both of these brainstem nuclei show peaks of cell proliferation, as indexed by increased numbers of cells labeled with BrdU, during metamorphic climax Simmons et al, 2006], the time period during which GAP-43 expression is also intense. A subset of these newly-born cells might form processes, and the formation of these processes might be reflected in increased GAP-43 expression.…”

Section: Possible Correlates With Developmental Changes In Functionmentioning

confidence: 99%

“…The nervous system of the bullfrog undergoes more dramatic changes over development than those seen in Xenopus , particularly in auditory/vestibular pathways, and thus we might expect dramatic changes in GAP-43 expression, as indexed by changes in intensity and distribution of immunolabeling, during bullfrog metamorphosis. We hypothesized that changes in expression in the auditory medulla and midbrain, areas which we have previously shown to undergo considerable anatomical and physiological changes over development [Boatright-Horowitz and Simmons, 1997;Chapman et al, 2006;Simmons et al, 2006;Horowitz et al, 2007a, b], would correlate with patterns of GAP-43 immunoreactivity. Further, we examined patterns of GAP-43 immunoreactivity in selected cranial nerves and in the forebrain, to determine if any changes in expression reflect a general process of growth and reorganization affecting the entire brain simultaneously, or if certain patterns of expression are temporally or spatially specific.…”

Section: Introductionmentioning

confidence: 99%

Developmental and Regional Patterns of GAP-43 Immunoreactivity in a Metamorphosing Brain

Simmons

Tanyu²,

Horowitz³

et al. 2008

Brain Behav Evol

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Growth-associated protein-43 is typically expressed at high levels in the nervous system during development. In adult animals, its expression is lower, but still observable in brain areas showing structural or functional plasticity. We examined patterns of GAP-43 immunoreactivity in the brain of the bullfrog, an animal whose nervous system undergoes considerable reorganization across metamorphic development and retains a strong capacity for plasticity in adulthood. Immunolabeling was mostly diffuse in hatchling tadpoles, but became progressively more discrete as larval development proceeded. In many brain areas, intensity of immunolabel peaked at metamorphic climax, the time of final transition from aquatic to semi-terrestrial life. Changes in intensity of GAP-43 expression in the medial vestibular nucleus, superior olivary nucleus, and torus semicircularis appeared correlated with stage-dependent functional changes in processing auditory stimuli. Immunolabeling in the Purkinje cell layer of the cerebellum and in the cerebellar nucleus was detectable at most developmental time points. Heavy immunolabel was present from early larval stages through the end of climax in the thalamus (ventromedial, anterior, posterior, central nuclei). Immunolabel in the tadpole telencephalon was observed around the lateral ventricles, and in the medial septum and ventral striatum. In postmetamorphic animals, immunoreactivity was confined mainly to the ventricular zones and immediately adjacent cell layers. GAP-43 expression was present in olfactory, auditory and optic cranial nerves throughout larval and postmetamorphic life. The continued expression of GAP-43 in brain nuclei and in cranial nerves throughout development and into adulthood reflects the high regenerative potential of the bullfrog’s central nervous system.

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Particle motion is broadly represented in the vestibular medulla of the bullfrog across larval development

Simmons

Flores

2011

J Comp Physiol A

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In their shallow-water habitats, bullfrog (Rana catesbeiana) tadpoles are exposed to both underwater and airborne sources of acoustic stimulation. We probed the representation of underwater particle motion throughout the tadpole’s dorsal medulla to determine its spatial extent over larval life. Using neurobiotin-filled micropipettes, we recorded neural activity to z-axis particle motion (frequencies of 40–200 Hz) in the medial vestibular nucleus, lateral vestibular nucleus, dorsal medullary nucleus (DMN), and along the dorsal arcuate pathway. Sensitivity was comparable in the medial and lateral vestibular nuclei, with estimated thresholds between 0.016 and 12.5 μm displacement. Neither best responding frequency nor estimated threshold varied significantly over larval stage. Transport of neurobiotin from active recording sites was also stable over development. The DMN responded poorly to z-axis particle motion, but did respond to low-frequency pressure stimulation. These data suggest that particle motion is represented widely and stably in the tadpole’s vestibular medulla. This is in marked contrast to the representation of pressure stimulation in the auditory midbrain, where a transient “deaf period” of non-responsiveness and decreased connectivity occurs immediately prior to metamorphic climax. We suggest that, in bullfrogs, sensitivity to particle motion and to pressure follows different developmental trajectories.

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Developmental changes in cell proliferation in the auditory midbrain of the bullfrog, Rana catesbeiana

Cited by 10 publications

References 46 publications

Cell Proliferation in the Forebrain and Midbrain of the Adult Bullfrog, <i>Rana catesbeiana</i>

Cell Proliferation in the Forebrain and Midbrain of the Adult Bullfrog, <i>Rana catesbeiana</i>

Developmental and Regional Patterns of GAP-43 Immunoreactivity in a Metamorphosing Brain

Particle motion is broadly represented in the vestibular medulla of the bullfrog across larval development

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