Distinct developmental dynamics of opposing persistent currents shape motoneuron firing during motor maturation of...

Zebrafish rapidly acquire new locomotor movements during the first few days of development. Rapid, ballistic movements relying on early-born primary motoneurons are supplemented with slower, more co-ordinated movements relying on later-born secondary motoneurons. We demonstrate distinct developmental dynamics of two persistent ionic currents related to locomotor rhythmogenesis in primary motoneurons during early development. From 2 to 5 days post-fertilization (dpf), a riluzole-sensitive persistent inward Na⁺ current associated with neural excitability gradually decreases in primary motoneurons. By contrast, the persistent outward potassium M-current peaks at 3 dpf and decreases afterwards. The influence of the M-current on the excitability and spike-frequency adaptation of primary motoneurons mirrors the non-monotonic developmental dynamics of its magnitude. Paired motoneuron-motor nerve recordings show different recruitment patterns of primary motoneurons at 3 vs. 5 dpf during light-evoked motor responses despite receiving similar synaptic drive. Modulation of the M-current during these responses shows that the M-current peak at 3 dpf shapes the activity pattern of primary motoneurons and consequent motor output. These findings thus reveal that rapid and precise changes in the intrinsic properties of spinal neurons enable motor control to mature appropriately in developing animals. KEY POINTS: Primary motoneurons express a persistent outward potassium current (M-current), as well as a persistent sodium current (I_NaP). During development, from 2 to 5 days post-fertilization (dpf), the amplitude of the persistent sodium current decreases. Across the same developmental period, the amplitude of the M-current increases transiently at 3 dpf before subsequently decreasing. As a consequence of these developmental changes, spike frequency adaptation and sustained firing in primary motoneurons changes between 2 and 5 dpf. The activity of primary motoneurons during light-evoked swimming is different between 3 and 5 dpf as a result of the changes in amplitude of the M-current.