Developmental transition of touch response from slow muscle-mediated coilings to fast muscle-mediated burst swimming in zebrafish

Abstract

It is well known that slow and fast muscles are used for long-term sustained movement and short bursts of activity, respectively, in adult animal behaviors. However, the contribution of the slow and fast muscles in early animal movement has not been thoroughly explored. In wild-type zebrafish embryos, tactile stimulation induces coilings consisting of 1–3 alternating contractions of the trunk and tail at 24hours postfertilization (hpf) and burst swimming at 48hpf. But, embryos defective in flightless I homolog (flii), which encodes for an actin-regulating protein, exhibit normal coilings at 24hpf that is followed by significantly slower burst swimming at 48hpf. Interestingly, actin fibers are disorganized in mutant fast muscle but not in mutant slow muscle, suggesting that slower swimming at 48hpf is attributable to defects of the fast muscle tissue. In fact, perturbation of the fast muscle contractions by eliminating Ca2+ release only in fast muscle resulted in normal coilings at 24hpf and slower burst swimming at 48hpf, just as flii mutants exhibited. In contrast, specific inactivation of slow muscle by knockdown of the slow muscle myosin genes led to complete loss of coilings at 24hpf, although normal burst swimming was retained by 48hpf. These findings indicate that coilings at 24hpf is mediated by slow muscle only, whereas burst swimming at 48hpf is executed primarily by fast muscle. It is consistent with the fact that differentiation of fast muscle follows that of slow muscle. This is the first direct demonstration that slow and fast muscles have distinct physiologically relevant contribution in early motor development at different stages.