Developmental changes in trigeminal motoneuron properties in the American bullfrog, Lithobates catesbeianus

In frogs, the neural circuits generating gill and lung ventilation are distinct, yet their activities converge on the same groups of motoneurons located in the brainstem, including the trigeminal, hypoglossal, and vagal motoneurons. Because lung ventilation requires more forceful contractions to “push” air back into the lungs, it is plausible that the basic electrophysiological properties of respiratory motoneurons that activate the buccal musculature change during tadpole development in ways that facilitate lung ventilation; however, this hypothesis remains untested. To address this issue we used an electrophysiological approach to compare the functional properties of trigeminal motoneurons between pre‐metamorphic tadpoles and adult frogs. Retrograde labelling of trigeminal motoneurons was performed with the fluorescent marker DiI at least 14 days prior to experiments. Using a coronal slice preparation, we performed whole‐cell recordings from fluorescently‐tagged cells to measure basic motoneurons properties. Electrophysiological characterization was performed by measuring membrane potential responses to steps of current injections. Unexpectedly, the trigeminal motor pool seemed to be composed of two distinct motoneuron populations based on cell size. Resting membrane potential did not differ between populations or developmental stages (~−54 mV). The smaller cells were generally more excitable than the larger ones as indicated by a lower rheobase (49 ± 7 versus 275 ± 48 pA) and a more hyperpolarized action potential threshold (−43 ± 2 versus −38 ± 2 mV). The density of the hyperpolarization‐activated inward current ( I h ) was more than 10 times greater in smaller cells. With regards to development, recordings revealed lower membrane resistance in frogs than tadpoles; this developmental change was more important in the smaller cells. Finally, the amplitude of evoked action potentials was greater in frog motoneurons than tadpoles; the developmental augmentation was more important in the smaller cells. While morphometric assessment of each cell type is underway, the cell heterogeneity observed in the trigeminal motor nucleus raises the possibility that the different cell types are associated with different motor commands (gill versus lung ventilation). Owing to the developmental changes observed in the smaller cells, we propose that this population is associated with the production of air breaths. Support or Funding Information Supported by Natural Sciences and Engineering Research Council of Canada