A behaviourally related developmental switch in nitrergic modulation of locomotor rhythmogenesis in larval Xenopus tadpoles
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Locomotor control requires functional flexibility to support an animal’s full behavioural repertoire. This flexibility is partly endowed by neuromodulators, allowing neural networks to generate a range of motor output configurations. In hatchling Xenopus tadpoles, before the onset of free swimming behaviour, the gaseous modulator nitric oxide (NO) inhibits locomotor output, shortening swim episodes and decreasing swim cycle frequency. While populations of nitrergic neurons are already present in the tadpole’s brainstem at hatching, neurons positive for the NO-synthetic enzyme, NOS, subsequently appear in the spinal cord suggesting additional as yet unidentified roles for NO during larval development. Here, we first describe the expression of locomotor behaviour during the animal’s change from an early sessile to a later free-swimming lifestyle and then compare the effects of NO throughout tadpole development. We identify a discrete switch in nitrergic modulation from net inhibition to overall excitation, coincident with the transition to free-swimming locomotion. Additionally, we show in isolated brainstem-spinal cord preparations of older larvae that NO's excitatory effects are manifest as an increase in the probability of spontaneous swim episode occurrence, as found previously for the neurotransmitter dopamine (DA), but that these effects are mediated within the brainstem. Moreover, while the effects of NO and DA are similar, the two modulators act in parallel rather than NO operating serially by modulating dopaminergic signalling. Finally, NO’s activation of neurons in the brainstem also leads to the release of NO in the spinal cord that subsequently contributes to NO’s facilitation of swimming.
Currie , S P , Combes , D , Scott , N W , Simmers , J & Sillar , K T 2016 , ' A behaviourally related developmental switch in nitrergic modulation of locomotor rhythmogenesis in larval Xenopus tadpoles ' Journal of Neurophysiology , vol. 115 , no. 3 , pp. 1446-1457 . https://doi.org/10.1152/jn.00283.2015
Journal of Neurophysiology
Copyright © 2016 the American Physiological Society Licensed under Creative Commons Attribution CC-BY 3.0 (http://creativecommons.org/licenses/by/3.0/deed.en_US)
DescriptionSupported by PICS (Projet International de Coopération Scientifique) of the French CNRS and a LabEx BRAIN Visiting Professorship to KTS. SPC was a BBSRC research student. NWS was an MPhil student supported in part by the E & RS Research Fund of the University of St Andrews.
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