Metamorphic Changes in GABA Immunoreactivity in the Brainstem of the Bullfrog, <i>Rana catesbeiana</i>

Abstract

We examined immunoreactivity for γ-aminobutyric acid (GABA) in auditory and vestibular brainstem nuclei of the bullfrog, Rana catesbeiana, across metamorphosis, a developmental period featuring significant anatomical and functional remodeling of the nervous system. In the early larval period, GABA-immunoreactive cell somata were visible in the vestibular nucleus complex and the torus semicircularis, as well as in the spinal cord, cerebellum and optic tectum. Fiber bundles such as the medial longitudinal fasciculus and the lemnsical pathways also exhibited intense label at these early stages. In contrast, only diffuse neuropil label was visible in the dorsolateral nucleus and the superior olivary nucleus at the same stages. This diffuse immunoreactivity became progressively more reduced over larval development, and stained somata were visible in these medullary nuclei by metamorphic climax stages. In the torus semicircularis, the numbers of labeled somata in both the developing laminar and principal nuclei increased over metamorphic development, and became progressively more organized into distinct layers. The adult pattern of GABA-like immunoreactivity in the auditory brainstem was reached by metamorphic climax stages, coincident with the maturation of the opercularis system, and preceding the final development of the external tympanum and the tympanic conduction pathway. The relatively earlier maturation of vestibular, compared to auditory, areas in the medulla might reflect the behavioral importance of vestibular-mediated motor reactions during tadpole life. The distribution of GABA in auditory brainstem nuclei in both developing and adult frogs is comparable to that observed in mammals and birds.

Distribution of GABA-Like Immunoreactive Cell Bodies in the Brains of Two Amphibians, <i>Rana catesbeiana</i> and <i>Xenopus laevis</i>

“…In addition to projecting to the torus semicircularis, the dorsal lateral nucleus projects to the superior olivary nucleus, which is reciprocally innervated with the major auditory nuclei in the anuran brain [Feng, 1986a, b]. Our findings are consistent with previous reports in bullfrogs, R. esculenta, and R. temporaria [Franzoni and Morino, 1989;Reichenberger et al, 1997;Simmons and Chapman, 2002]. In R. pipiens, GABAergic inhibition via the GABA A receptor can shape the frequency tuning of neurons and modify the response properties of the superior olivary nucleus [Zheng and Hall, 2000].…”

“…Cells immunoreactive for GABA have previously been reported in the magnocellular nucleus (ventral torus semicircularis) and laminar nucleus of three anuran species including Xenopus [Endepols et al, 2000]. On the other hand, the bullfrog toral magnocellular nucleus has been previously described as devoid of GABA-immunoreactive somata [Simmons and Chapman, 2002]. The presence of GABA in the torus semicircularis has also been found in the auditory systems of other vertebrate classes including a teleost [Medina et al, 1994], a reptile [Bennis et al, 1991], and in the inferior colliculus (homologous to torus) of birds [Carr et al, 1989] and mammals [Vater et al, 1992].…”

“…The distribution of GABA in the brain of developing Xenopus laevis has been thoroughly mapped but expression in some brain areas is transient so the adult pattern can differ significantly [Roberts et al, 1987;Barale et al, 1996]. GABA immunoreactivity has also been described in the brainstem of developing bullfrog (Rana catesbeiana) tadpoles but the pattern of neurotransmitter expression across the rest of the brain was not reported [Simmons and Chapman, 2002]. Particular GABAergic systems have been studied independently in some anurans.…”

“…The visual system, for example, has been the emphasis of many reports (see Discussion). Where species comparisons can be made (e.g., in the anuran optic tectum), significant differences in the pattern of GABA-immunoreactivity have been found [Rybicka and Udin, 1994;Gabriel and Straznicky, 1995;Simmons and Chapman, 2002]. Species differences might well exist in other areas of the anuran brain but this is unknown.…”

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

“…In the tadpole brain, these subdivisions cannot be easily identified because of differences in cell density and patterns of lamination across development. For example, the area described in adults as the principal nucleus does not attain its distinctive pattern of lamination until metamorphic climax stages [Simmons and Chapman, 2002]. Moreover, until metamorphic climax stages, the optic ventricle and aqueduct of Sylvius are continuous from the level of the nucleus isthmus up to the level of the oculomotor nucleus [Kumaresan et al, 1998; fig.…”