Corticosterone promotes emergence of fictive air breathing in Xenopus laevis Daudin tadpole brainstems

Abstract

SUMMARY The emergence of air breathing during amphibian metamorphosis requires significant changes to the brainstem circuits that generate and regulate breathing. However, the mechanisms controlling this developmental process are unknown. Because corticosterone plays an important role in the neuroendocrine regulation of amphibian metamorphosis, we tested the hypothesis that corticosterone augments fictive air breathing frequency in Xenopus laevis. To do so, we compared the fictive air breathing frequency produced by in vitro brainstem preparations from pre-metamorphic tadpoles and adult frogs before and after 1 h application of corticosterone (100 nmol l–1). Fictive breathing measurements related to gill and lung ventilation were recorded extracellularly from cranial nerve rootlets V and X. Corticosterone application had no immediate effect on respiratory-related motor output produced by brainstems from either developmental stage. One hour after corticosterone wash out, fictive lung ventilation frequency was increased whereas gill burst frequency was decreased. This effect was stage specific as it was significant only in preparations from tadpoles. GABA application (0.001–0.5 mmol l–1) augmented fictive air breathing in tadpole preparations. However, this effect of GABA was no longer observed following corticosterone treatment. An increase in circulating corticosterone is one of the endocrine processes that orchestrate central nervous system remodelling during metamorphosis. The age-specific effects of corticosterone application indicate that this hormone can act as an important regulator of respiratory control development in Xenopus tadpoles. Concurrent changes in GABAergic neurotransmission probably contribute to this maturation process, leading to the emergence of air breathing in this species.