Evolutionary Divergence in Developmental Strategies and Neuromodulatory Control Systems of Two Amphibian Locomotor Networks1

SYNOPSIS. Attempts to understand the neural mechanisms which produce behaviour must consider both prevailing sensory cues and the central cellular and synaptic changes they direct. At each level, neuromo-dulation can additionally shape the final output. We have investigated neuromodulation in the developing spinal motor networks in hatchling tadpoles of two closely related amphibians, Xenopus laevis and Rana temporaria to examine the subtle differences in their behaviours that could be attributed to their evolutionary divergence. At the point of hatching, both species can swim in response to a mechanosensory stimulus, however Rana embryos often display a more forceful, non-locomotory coiling behaviour. Whilst the synaptic drive that underlies these behaviours appears similar, subtle inter-specific differences in neuronal properties shape motor outputs in different ways. For example, Rana neurons express N-methyl-D-aspartate (NMDA)/sero-tonin (5-HT)-dependent oscillations, not present in hatchling Xenopus and many also exhibit a prominent slow spike after-hyperpolarisation. Such properties may endow the spinal circuitry of Rana with the ability to produce a more flexible range of outputs. Finally, we compare the roles of the neuromodulators 5-HT, noradrenaline (NA) and nitric oxide (NO) in shaping motor outputs. 5-HT increases burst durations during swimming in both Xenopus and Rana, but 5-HT dramatically slows the cycle period in Rana with little effect in Xenopus. Three distinct, but presumably homologous NO-containing brainstem clusters of neurons have been described, yet the effects of NO differ between species. In Xenopus, NO slows and shortens swimming in a manner similar to NA, yet in Rana NO and NA elicit the non-rhythmic coiling pattern