Synaptic drive to motoneurons during fictive swimming in the developing zebrafish

The development of swimming behavior and the correlated activity patterns r ecorded in motoneurons during fictive swimming in paralyzed zebrafish larva e were examined and compared. Larvae were studied from when they hatch (aft er 2 days) and are first capable of locomotion to when they are active swim mers capable of capturing prey (after 4 days). High-speed (500 Hz) video im aging was used to make a basic behavioral characterization of swimming. At hatching and up to day 3, the larvae swam infrequently and in an undirected fashion. They displayed sustained bursts of contractions ('burst swimming' ) at an average frequency of 60-70 Hz that lasted from several seconds to a minute in duration. By day 4 the swimming had matured to a more frequent a nd less erratic "beat-and-glide" mode, with slower (similar to 35 Hz) beats of contractions for similar to 200 ms alternating with glides that were tw ice as long, lasting from just a few cycles to several minutes overall. In whole cell current-clamp recordings, motoneurons displayed similar excitato ry synaptic activity and firing patterns, corresponding to either fictive b urst swimming (day 2-3) or beat-and-glide swimming (day 4). The resting pot entials were similar at all stages (about -70 mV) and the motoneurons were depolarized (to about -40 mV) with generally non-overshooting action potent ials during fictive swimming. The frequency of sustained inputs during fict ive burst swimming and of repetitive inputs during fictive beat-and glide s wimming corresponded to the behavioral contraction patterns. Fictive swimmi ng activity patterns were eliminated by application of glutamate antagonist s (kynurenic acid or 6-cyano-7-nitroquinoxalene- 2,3-dione and DL-2-amino-5 -phosphonovaleric acid) and were modified but maintained in the presence of the glycinergic antagonist strychnine. The corresponding synaptic currents underlying the synaptic drive to motoneurons during fictive swimming could be isolated under voltage clamp and consisted of cationic [glutamatergic p ostsynaptic currents (PSCs)] and anionic inputs (glycinergic PSCs). Either sustained or interrupted patterns of PSCs were observed during fictive burs t or beat-and-glide swimming, respectively. During beat-and-glide swimming, a tonic inward current and rhythmic glutamatergic PSCs (similar to 35 Hz) were observed. In contrast, bursts of glycinergic PSCs occurred at a higher frequency, resulting in a more tonic pattern with little evidence for sync hronized activity. We conclude that a rhythmic glutamatergic synaptic drive underlies swimming and that a tonic, shunting glycinergic input acts to mo re closely match the membrane time constant to the fast synaptic drive.