The development of swimming rhythmicity in post-embryonic Xenopus laevis

Abstract

The post-embryonic development of 'fictive' swimming in immobilized Xenopus laevis tadpoles has been examined during the first day of larval life. In Xenopus embryos (stage 37-38; Nieuwkoop & Faber 1956), the rhythmic ventral root activity underlying swimming occurs as single brief (ca. 7 ms) compound impulses on each cycle. However, by stage 42 (about 24 h after hatching), ventral root discharge consists of bursts lasting around 20 ms per cycle. In addition to increased burst duration in each cycle of larval swimming, the range of cycle periods within an episode increases, although mean period values (ca. 70-80 ms) remain similar to those of the younger animal. Consequently, motoneurons at developmental stage 42 are active during swimming for a greater percentage (ca. 25%) of cycle time than at stage 37-38 (ca. 10%). Developmental stage 40 (ca. 12 h post-hatching) is an intermediate stage in rhythm development. Ventral root discharge varies from bursts of 10-20 ms at the start of an episode to embryonic (ca. 7 ms) spikes at the end of an episode. Furthermore, discharge varies from bursts of activity in rostral segments of stage 40 larvae to 7 ms spikes more caudally, as in embryos. The data thus suggest that Xenopus swimming rhythmicity develops relatively rapidly, along a rostrocaudal gradient, and may involve acquisition of multiple spiking in spinal neurons.

Developmental changes in head movement kinematics during swimming inXenopus laevistadpoles

“…As previous reports on swimming X. laevis hatchlings reported that the frequency of the head/tail oscillations decreased gradually over the course of a given swimming episode Sillar and Roberts, 1993;Sillar et al, 1991), the difference between the mean frequency of the first two and the last two half-cycles of each episode was calculated ( Fig. 4B; 221 episodes in N=25 animals) and found not to be significantly different from zero (one-sample Wilcoxon signed-rank test, P>0.05).…”

“…While mostly attached to a substrate between stages 37 and 38 (Boothby and Roberts, 1992; Jamieson and Roberts, 2000), the propensity of Xenopus larvae to spontaneously swim freely increases after the onset of active feeding at stage 45 (Nieuwkoop and Faber, 1956), as confirmed by a developmental study on fictively swimming animals (Currie et al, 2016). At this time, the frequency of the tail undulations is generally high (10-25 Hz; and each swimming bout is characterised by decreasing frequencies over the course of the episode Sillar and Roberts, 1993;Sillar et al, 1991). This contrasts with the observation in the older and thus larger tadpoles studied here, where the swimming frequency remains largely constant throughout a given episode (Fig.…”

“…Most of the difference in the magnitude of swimming-related head dynamics between Xenopus and zebrafish is probably due to the substantially higher swimming frequency in the latter species, which reaches up to 70 Hz (see above). As larval Xenopus hatchlings also swim with a higher frequency than older and thus larger larvae (Sillar et al, 1991), it is likely that higher angular velocities are regularly reached.…”

Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord

“…In this way, inhibition from aINs may also help to synchronize the firing of CPG neurons on the same side and lead indirectly to better alternation between the two sides. aIN inhibition may become more important later in development when Xenopus motoneuron fire multiply on each cycle of swimming (Sillar et al, 1991). In the case of sensory pathway dlc interneurons, aIN inhibition gates the flow of sensory input so that reflex responses are modulated to fit with ongoing swimming activity Roberts, 1988, 1992;Li et al, 2002).…”

Developmental changes in expression of ion currents accompany maturation of locomotor pattern in frog tadpoles

“…Xenopus embryos and larvae were prepared for extracellular ventral root recordings in accordance with the UK Animals (Scientific Procedures) Act, 1986, using previously described methods (Sillar et al 1991;Dale, 1995b). Drug access was facilitated by bilateral removal of the rostral myotomes and loosening the dorsal attachment of the remaining myotomes.…”