Hypoxia Induces Emergence of Adult‐like Respiratory Motor Patterns in Pre‐metamorphic Bullfrog Brainstem Preparations

Abstract

Vertebrate respiratory development involves the gradual transformation of primal respiratory behaviours into mature forms with specific, measurable characteristics. Yet, the impacts of environmental factors on respiratory maturation remain enigmatic. In pre‐metamorphic tadpoles of Lithobates catesbeianus (American bullfrog), gill ventilation predominates, while lung breathing is rarely observed. Following metamorphosis, lung breathing emerges as the dominant respiratory behaviour. Since accelerated metamorphosis (including respiratory development) constitutes an adaptive response to deterioration of the milieu, we hypothesized that hypoxia is sufficient to accelerate maturation of the motor command for lung breathing. Specifically, we predicted that hypoxia would elicit an “adult‐like” motor pattern in pre‐metamorphic tadpoles, including high amplitude lung bursts occurring episodically with a “ramping up” of burst amplitude within episodes. Using early‐stage tadpoles (Taylor‐Kollros: VI–IX), we recorded respiratory motor activity from cranial nerves V, VII and X in isolated brainstems before, during, and 2h after exposure to 15 min of moderate hypoxia (PwO2 range: 45–76 Torr). To test for long‐term effects brainstems were then incubated overnight in oxygenated artificial cerebral spinal fluid at 17°C and motor activity recorded 24h post‐hypoxia. In line with our predictions, lung motor activity in brainstems exposed to hypoxia exhibited characteristics of adult breathing while that of time‐matched controls resembled typical tadpoles. Lung burst amplitude was increased relative to baseline (+90%) at 2h post‐hypoxia. Additionally, hypoxia increased the incidence of lung burst episodes more than 300%, with a concurrent increase in the number of breaths per episode from an average of 2.2 at baseline to 3.3 at 2h post‐hypoxia (controls: 1.9 at 2h). The “ramping up” of lung burst amplitude during episodes was variable over time but gradually increased in prevalence above control levels by 24h post‐hypoxia. These data demonstrate that central hypoxia induces the emergence of “adult‐like” lung motor patterns in early pre‐metamorphic tadpoles.Support or Funding InformationThis work was supported by a Fonds de Recherche du Québec ‐ Santé (FRQS) Collaborative Scholarship awarded to T. Janes and an NSERC Discovery Grant awarded to R. Kinkead.This abstract is from the Experimental Biology 2019 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.