Ontogeny of central O2 chemoreception: the hypoxic response in the brainstem of developing frogs

Abstract

Central O2 chemoreception was assessed in tadpoles of varying developmental stages and frogs (Rana catesbeiana). Brainstems were removed en bloc from anesthetized animals and neuroventilatory gill and lung bursts were recorded from the facial and hypoglossal nerves at their exit points from the brainstem. Recordings were made while each brainstem was superfused with normoxic or hypoxic artificial cerebrospinal fluid (aCSF). Superfusion of the brainstem with hypoxic aCSF elicited an increase in fictive lung ventilation across all stages of development. Early- and late-stage tadpoles showed burst frequency increases in the 1st hour of hypoxia, while frequency decreased with prolonged hypoxia. Middle-stage tadpoles exhibited increased burst frequency in the 3rd hour of hypoxia. Gill burst frequency remained constant throughout 3h of hypoxic exposure in all developmental stages. Therefore, like the central hypercapnic response, the central hypoxic response manifests as an increase in lung ventilation in tadpoles. Some tadpole brainstems became apneic (total loss of gill and lung bursts); however, this event was rare. Superfusion of frog brainstems with hypoxic aCSF elicited an increase in lung burst frequency during the 1st hour of hypoxia and a decrease during continued hypoxia. Apnea was common among frog brainstems exposed to prolonged hypoxia. Most brainstems, tadpole and adult, regained rhythm after the 3-hour hypoxic exposure when normoxic superfusion was re-instated. This study characterized the hypoxic response of R catesbeiana as an increase in neuroventilatory lung bursts with a decrease during prolonged exposure common among adults. Frogs and tadpoles were also shown to be highly hypoxia tolerant. Funded by NIH-NINDS 2U54NS041069-06AI.