The development of free-swimming in Xenopus laevis larvae

Abstract

In Xenopus laevis frog tadpoles, highly self-motive, free-swimming behaviour emerges at the onset of feeding. This is in contrast to the earlier post-hatched larval form, which is capable of escape swimming when stimulated, but normally lies dormant.

This developmental transition in behaviour has been documented here and studied in a semi-intact preparation developed to examine the motor output from larvae at the onset of filter feeding. There is a progressive increase in spontaneous motor activity during this period, where spontaneous fictive swimming occurs in episodes of variable duration but with significantly larger burst durations. This spontaneous activity persists after removal of both the fore- and midbrain, but is absent in spinalised preparations. The spontaneous activity is similar to NMDA (100µM) induced rhythm but shows greater periodic variability in the frequency and occurrence of swimming activity. The activity is not dependent on inhibitory synaptic transmission, but is under the control of central GABAergic restraint, as blocking this inhibition with bicuculine (10µM) increased spontaneous locomotor activity. This is distinct to the role of glycinergic inhibition which influences the character of the ventral root bursts, as strychnine (5µM) caused an initial increase in frequency before bursts were synchronised on both the left and right sides, but not the presence of spontaneous activity. However, activity is abolished by the persistent sodium current blocker riluzole (5µM) and enhanced by veratridine (90nM) which potentiates the current, which may suggest that it originates in neurons with pacemaker-like properties - possibly within the hindbrain.

Evidence is also provided which shows that the neuromodulatory gas nitric oxide becomes an excitatory modulator of the Xenopus swimming network at the onset of a free-swimming existence, switching from having a global inhibitory role on locomotion in early larval life. The nitric oxide donor DEA/NO (200µM) increased spontaneous fictive swimming in the semi-intact preparation. In contrast, the nitric oxide synthase inhibitor L-NAME combined with PTIO, which sequesters nitric oxide, decreased spontaneous fictive swimming.

It is proposed that the emergence of this rhythmic, spontaneous motor activity parallels the increase in swimming at the onset of feeding, suggesting a direct behavioural role for spontaneous network activity in the developing animal.