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

Horowitz, Seth S.; Simmons, Andrea Megela

doi:10.1016/j.brainres.2007.04.078

Cited by 4 publications

(4 citation statements)

References 20 publications

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“…Anatomical boundaries and terminology are consistent with those described for developing Horowitz et al, 2007a;Horowitz and Simmons, 2007] and adult Opdam et al, 1976;Wilczynski and Northcutt, 1983;Marín et al, 1997] ranid brains. Atlases of the tadpole brain at medullary, mesencephalic, and diencephalic levels have been published previously .…”

Section: Western Blotmentioning

confidence: 61%

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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Section: Western Blotmentioning

confidence: 61%

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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“…The OT of bullfrog tadpoles does not clearly show 6 distinct layers until around stages 26-28, during the early larval period [Horowitz and Simmons, 2007]. Throughout the rest of larval development, deep layers are more densely packed than superficial layers and comprise a relatively larger proportion of overall tectal depth than seen in postmetamorphic frogs.…”

Section: Injection Sites and Nomenclaturementioning

confidence: 97%

“…The developmental variability in tectal lamination [Horowitz and Simmons, 2007] prevented restricted injections to any individual layer. Our results are based primarily on injections placed at mid-levels of the OT; we performed very few injections centered at very rostral levels of the OT, and we made no injections at caudal levels of the OT.…”

Section: Discussionmentioning

confidence: 99%

Development of Tectal Connectivity across Metamorphosis in the Bullfrog (Rana catesbeiana)

Horowitz

Simmons

2010

Brain Behav Evol

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In the bullfrog (Rana catesbeiana), the process of metamorphosis culminates in the appearance of new visual and visuomotor behaviors reflective of the emergence of binocular vision and visually-guided prey capture behaviors as the animal transitions to life on land. Using several different neuroanatomical tracers, we examined the substrates that may underlie these behavioral changes by tracing the afferent and efferent connectivity of the midbrain optic tectum across metamorphic development. Intratectal, tectotoral, tectotegmental, tectobulbar, and tecto-thalamic tracts exhibit similar trajectories of neurobiotin fiber label across the developmental span from early larval tadpoles to adults. Developmental variability was apparent primarily in intensity and distribution of cell and puncta label in target nuclei. Combined injections of cholera toxin subunit β and Phaseolus vulgaris leucoagglutinin consistently label cell bodies, puncta, or fiber segments bilaterally in midbrain targets including the pretectal gray, laminar nucleus of the torus semicircularis, and the nucleus of the medial longitudinal fasciculus. Developmentally stable label was observed bilaterally in medullary targets including the medial vestibular nucleus, lateral vestibular nucleus, and reticular gray, and in forebrain targets including the posterior and ventromedial nuclei of the thalamus. The nucleus isthmi, cerebellum, lateral line nuclei, medial septum, ventral striatum, and medial pallium show more developmentally variable patterns of connectivity. Our results suggest that even during larval development, the optic tectum contains substrates for integration of visual with auditory, vestibular, and somatosensory cues, as well as for guidance of motivated behaviors.

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“…The frog’s brain as a whole alters considerably in size and organization over metamorphosis (Horowitz & Simmons, 2007), reflecting developmental changes in both external (emergence of limbs, degeneration of the lateral line sensory organs in terrestrial frogs) and internal (progressive development of the inner and middle ears) morphology. These dynamic alterations in brain structure are manifested in changes in the size and spatial position of auditory nuclei, in the neurochemical organization of these nuclei, and in modifications of connectivity between these nuclei.…”

Section: Development Of Ascending Auditory Pathwaysmentioning

confidence: 99%

Tadpole bioacoustics: Sound processing across metamorphosis.

Simmons¹

2019

Behavioral Neuroscience

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Many species of anuran amphibians (frogs and toads) undergo metamorphosis, a developmental process during which external and internal body morphologies transform dramatically as the animal transitions to a new ecosystem (from aquatic to terrestrial) and develops new behavior patterns (from filter-feeding to active pursuit of moving prey; from mostly mute to highly vocal). All sensory systems transform to some extent during metamorphosis, even in those “primitive” anuran species that remain fully aquatic in adult life. In this article, I review what is known about the development of the auditory system in anuran tadpoles. I identify crucial developmental windows for major maturational events in the ear and brainstem that showcase the structural and physiological reorganization of the substrates for hearing airborne sounds as the animal navigates the metamorphic transition. I argue that auditory development is dynamic and nonlinear, and I point out areas for future investigation. Understanding metamorphosis can shed light on how organisms adapt to major environmental challenges.

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

Cited by 4 publications

References 20 publications

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

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

Development of Tectal Connectivity across Metamorphosis in the Bullfrog (Rana catesbeiana)

Tadpole bioacoustics: Sound processing across metamorphosis.

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