A gradient in endogenous rhythmicity and oscillatory drive matches recruitment order in an axial motor pool

The rhythmic firing behavior of spinal motoneurons is a function of their electrical properties and synaptic inputs. However, the relative contribution of endogenous versus network-based rhythmogenic mechanisms to locomotion is unclear. To address this issue, we have recorded from identified motoneurons and compared their current-evoked firing patterns to network-driven ones in the larval zebrafish (Danio rerio). Zebrafish axial motoneurons are recruited topographically from the bottom of the spinal cord up. Here, we have explored differences in the morphology of axial motoneurons, their electrical properties, and their synaptic drive, to reveal how they match the topographic pattern of recruitment. More ventrally located "secondary" motoneurons generate bursts of action potentials in response to constant current steps, demonstrating a strong inherent rhythmogenesis. The membrane potential oscillations underlying bursting behavior occur in the normal frequency range of swimming. In contrast, more dorsal secondaries chatter in response to current, while the most dorsally distributed "primary" motoneurons all fire tonically. We find that systematic variations in excitability and endogenous rhythmicity are inversely related to the level of oscillatory synaptic drive within the entire axial motor pool. Specifically, bursting cells exhibit the least amount of drive, while tonic cells exhibit the most. Our data suggest that increases in swimming frequency are accomplished by the recruitment of axial motoneurons that progressively rely on instructive synaptic drive to shape their oscillatory activity appropriately. Thus, within the zebrafish spinal cord, there are differences in the relative contribution of endogenous versus network-based rhythms to locomotion and these vary predictably according to order of recruitment.