Respiratory motoneuron properties during the transition from gill to lung breathing in the American bullfrog.

TitleRespiratory motoneuron properties during the transition from gill to lung breathing in the American bullfrog.
Publication TypeJournal Article
Year of Publication2019
AuthorsJanes, TA, Fournier, S, Chamberland, S, Funk, GD, Kinkead, R
JournalAm J Physiol Regul Integr Comp Physiol
Date Published2019 Jan 02
ISSN1522-1490
Abstract

Amphibian respiratory development involves a dramatic metamorphic transition from gill- to lung-breathing, and coordination of distinct motor outputs. To determine whether the emergence of adult respiratory motor patterns was associated with similarly dramatic changes in motoneuron (MN) properties, we characterized the intrinsic electrical properties of American bullfrog trigeminal MNs innervating respiratory muscles comprising the buccal pump. In pre-metamorphic tadpoles (TK stages IX-XVIII) and adult frogs, morphometric analyses and whole-cell recordings were performed in trigeminal MNs identified using fluorescent retrograde labeling. Two MN subtypes (I and II) were identified in tadpoles and adults based on the amplitude of the depolarizing sag induced by hyperpolarizing voltage steps. Compared to Type II MNs, Type I MNs had larger sag amplitudes (suggesting a larger hyperpolarization activated inward current, I), greater input resistance, lower rheobase, hyperpolarized action potential threshold, steeper f/I relationships, fast firing rates and received fewer EPSCs. Post-metamorphosis, Type I MNs exhibited similar sag, enhanced post-inhibitory rebound and increased action potential amplitude with a smaller magnitude fast afterhyperpolarization. Compared to tadpoles, Type II MNs from frogs received higher frequency - larger amplitude EPSCs. Input resistance decreased and rheobase increased post-metamorphosis in all MNs, concurrent with increased soma area and hyperpolarized action potential threshold. We suggest that Type I MNs are likely recruited in response to smaller, buccal-related synaptic inputs as well as larger lung-related inputs, while Type II MNs are likely recruited in response to stronger synaptic inputs associated with larger buccal breaths, lung breaths or non-respiratory behaviors involving powerful muscle contractions.

DOI10.1152/ajpregu.00303.2018
Alternate JournalAm. J. Physiol. Regul. Integr. Comp. Physiol.
PubMed ID30601705