Developmental Maturation of Functional Coupling Between Ventilatory Oscillators in the American Bullfrog

Many vital motor behaviors - including locomotion, swallowing, and breathing - appear to be dependent upon the activity of and coordination between multiple endogenously rhythmogenic nuclei, or neural oscillators. Much as the functional development of sensory circuits is shaped during maturation, we hypothesized that coordination of oscillators involved in motor control may likewise be maturation-dependent, i.e., coupling and coordination between oscillators change over development. We tested this hypothesis using the bullfrog isolated brainstem preparation to study the metamorphic transition of ventilatory motor patterns from early rhythmic buccal (water) ventilation in the tadpole to the mature pattern of rhythmic buccal and lung (air) ventilation in the adult. Spatially distinct oscillators drive buccal and lung bursts in the isolated brainstem; we found these oscillators to be active but functionally uncoupled in the tadpole. Over the course of metamorphosis, the rhythms produced by the buccal and lung oscillators become increasingly tightly coordinated. These changes parallel the progression of structural and behavioral changes in the animal, with adult levels of coupling arising by the metamorphic stage (forelimb eruption). These findings suggest that oscillator coupling undergoes a maturation process similar to the refinement of sensory circuits over development.