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A behaviorally related developmental switch in nitrergic modulation of locomotor rhythmogenesis in larval Xenopus tadpoles

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Currie_2016_JN_BehaviourallyRelated_CCBY.pdf (975.8Kb)
Date
03/2016
Author
Currie, Stephen Paul
Combes, Denis
Scott, Nicholas William
Simmers, John
Sillar, Keith Thomas
Keywords
Locomotion
Tadpole
Development
Nitric oxide
Modulation
BF Psychology
NDAS
BDC
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Abstract
Locomotor control requires functional flexibility to support an animal's full behavioral 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 behavior, 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 brain stem at hatching, neurons positive for the NO-synthetic enzyme, NO synthase, 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 behavior 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 brain stem-spinal cord preparations of older larvae that NO's excitatory effects are manifested as an increase in the probability of spontaneous swim episode occurrence, as found previously for the neurotransmitter dopamine, but that these effects are mediated within the brain stem. Moreover, while the effects of NO and dopamine are similar, the two modulators act in parallel rather than NO operating serially by modulating dopaminergic signaling. Finally, NO's activation of neurons in the brain stem also leads to the release of NO in the spinal cord that subsequently contributes to NO's facilitation of swimming.
Citation
Currie , S P , Combes , D , Scott , N W , Simmers , J & Sillar , K T 2016 , ' A behaviorally 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
Publication
Journal of Neurophysiology
Status
Peer reviewed
DOI
https://doi.org/10.1152/jn.00283.2015
ISSN
0022-3077
Type
Journal article
Rights
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)
Description
Supported 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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  • University of St Andrews Research
URI
http://hdl.handle.net/10023/8559

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