Developmental and regional expression of NADPH‐diaphorase/nitric oxide synthase in spinal cord neurons correlates with the emergence of limb motor networks in metamorphosing <i>Xenopus laevis</i>

Ramanathan, Sankari; Combes, Denis; Molinari, Micol; Simmers, John; Sillar, Keith T.

doi:10.1111/j.1460-9568.2006.05057.x

Cited by 21 publications

(16 citation statements)

References 45 publications

(86 reference statements)

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“…In our work, the number of NO-PC were increased in the spinal cord segments corresponding to brachial and sacral plexuses and also at the beginning of the tail and this could be due to the fact that salamanders are tetrapods capable of both swimming and walking (ten Donkelaar et al, 2001). Our finding is antagonistic with Ramanathan et al (2006), who showed that during early stages of metamorphosis, nitrergic neurons were excluded from regions where spinal limb circuits were forming. As metamorphosis progressed, NOS expression became distributed along the length of the spinal cord together with an increase in the number and intensity of labeled cells and fibers.…”

Section: Discussioncontrasting

confidence: 87%

Distribution of nitric oxide-producing cells along spinal cord in urodeles

Mahmoud

Fahmy

Moftah

et al. 2014

Front. Cell. Neurosci.

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Nitric oxide is a unique neurotransmitter, which participates in many physiological and pathological processes in the organism. There are little data about the neuronal nitric oxide synthase immunoreactivity in the spinal cord of amphibians. In this respect, the present study aims to investigate the distribution of nitric oxide producing cells in the spinal cord of urodele and to find out the possibility of a functional locomotory role to this neurotransmitter. The results of the present study demonstrate a specific pattern of NADPH-d labeling in the selected amphibian model throughout the spinal cord length as NADPH-d-producing cells and fibers were present in almost all segments of the spinal cord of the salamander investigated. However, their number, cytological characteristics and labeling intensity varied significantly. It was noticed that the NO-producing cells (NO-PC) were accumulated in the ventral side of certain segments in the spinal cord corresponding to the brachial and sacral plexuses. In addition, the number of NO-PC was found to be increased also at the beginning of the tail and this could be due to the fact that salamanders are tetrapods having bimodal locomotion, namely swimming and walking.

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Section: Discussioncontrasting

confidence: 87%

Distribution of nitric oxide-producing cells along spinal cord in urodeles

Mahmoud

Fahmy

Moftah

et al. 2014

Front. Cell. Neurosci.

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“…Neuronal NOS (nNOS) immunocytochemistry was performed using protocols developed previously for Xenopus (Ramanathan et al, 2006). The isolated lamprey spinal cord was fixed in 4% paraformaldehyde, pH 7.4, overnight at room temperature, washed in 0.1 M PB (3 ϫ 10 min).…”

Section: Methodsmentioning

confidence: 99%

Nitric Oxide Potentiation of Locomotor Activity in the Spinal Cord of the Lamprey

Kyriakatos¹,

Molinari²,

Mahmood³

et al. 2009

J. Neurosci.

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To understand the intrinsic operation of spinal networks generating locomotion, we need to not only characterize the constituent neurons and their connectivity, but also determine the role of intrinsic modulation in shaping the final motor output. We have focused on the effects of nitric oxide (NO) on the locomotor frequency and the underlying synaptic mechanisms in the lamprey spinal cord. To identify the source of NO, we used NADPH-diaphorase histochemistry and nNOS immunocytochemistry. Gray matter and sensory neurons were positively labeled using both methods. Preparations preincubated with NO synthase inhibitors displayed slower locomotor frequency that increased upon washout of the inhibitors, suggesting that NO is an endogenous neuromodulator in the spinal cord. Application of NO donors increased the locomotor frequency that was blocked by an NO scavenger and partially reduced by an inhibitor of sGC. To analyze the synaptic modulation underlying the NO-induced increase of the locomotor frequency we performed intracellular recordings from motoneurons and interneurons. The NO-induced increase in locomotor frequency was associated with a decrease in the midcycle inhibition and an increase in on-cycle excitation. To determine the site of action of NO, we examined the effect of NO donors on miniature PSCs. NO increased both the frequency and amplitude of mEPSCs while it only decreased the frequency of mIPSCs, suggesting the increased excitation is mediated by both presynaptic and postsynaptic mechanisms, while the decrease in inhibition involves only presynaptic mechanisms. Our results demonstrate a significant role of NO in adult vertebrate motor control which, via modulation of both excitatory and inhibitory transmission, increases the locomotor burst frequency.

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“…Comparisons of the "fictive" locomotor patterns generated by in vitro preparations at different metamorphic stages have begun to unravel how the developmental remodelling of spinal locomotor circuitry is achieved (Combes et al, 2004), with the eventual aim of determining the neurobiological substrates of such plasticity at the cellular and systems levels. We have also reported that during metamorphosis, neurons that produce the gaseous neuromodulator, nitric oxide (NO), are distributed in a spatial and temporal pattern appropriate for a developmental role in the assembly of the limb motor circuitry (Ramanathan et al, 2006). Preliminary results have also suggested that NO exerts modulatory actions on the expression of spinal locomotor output throughout this period.…”

Section: Introductionmentioning

confidence: 99%

Development and neuromodulation of spinal locomotor networks in the metamorphosing frog

Rauscent

Ray

Cabirol-Pol

et al. 2006

Journal of Physiology-Paris

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Metamorphosis in the anuran frog, Xenopus laevis, involves profound structural and functional transformations in most of the organism's physiological systems as it encounters a complete alteration in body plan, habitat, mode of respiration and diet. The metamorphic process also involves a transition in locomotory strategy from axial-based undulatory swimming using alternating contractions of left and right trunk muscles, to bilaterally-synchronous kicking of the newly developed hindlimbs in the young adult. At critical stages during this behavioural switch, functional larval and adult locomotor systems co-exist in the same animal, implying a progressive and dynamic reconfiguration of underlying spinal circuitry and neuronal properties as limbs are added and the tail regresses. To elucidate the neurobiological basis of this developmental process, we use electrophysiological, pharmacological and neuroanatomical approaches to study isolated in vitro brain stem/spinal cord preparations at different metamorphic stages. Our data show that the emergence of secondary limb motor circuitry, as it supersedes the primary larval network, spans a developmental period when limb circuitry is present but not functional, functional but co-opted into the axial network, functionally separable from the axial network, and ultimately alone after axial circuitry disappears with tail resorption. Furthermore, recent experiments on spontaneously active in vitro preparations from intermediate metamorphic stage animals have revealed that the biogenic amines serotonin (5-HT) and noradrenaline (NA) exert short-term adaptive control over circuit activity and inter-network coordination: whereas bath-applied 5-HT couples axial and appendicular rhythms into a single unified pattern, NA has an opposite decoupling effect. Moreover, the progressive and region-specific appearance of spinal cord neurons that contain another neuromodulator, nitric oxide (NO), suggests it plays a role in the maturation of limb locomotor circuitry. In summary, during Xenopus metamorphosis the network responsible for limb movements is progressively segregated from an axial precursor, and supra- and intra-spinal modulatory inputs are likely to play crucial roles in both its functional flexibility and maturation.

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Developmental and regional expression of NADPH‐diaphorase/nitric oxide synthase in spinal cord neurons correlates with the emergence of limb motor networks in metamorphosing Xenopus laevis

Cited by 21 publications

References 45 publications

Distribution of nitric oxide-producing cells along spinal cord in urodeles

Distribution of nitric oxide-producing cells along spinal cord in urodeles

Nitric Oxide Potentiation of Locomotor Activity in the Spinal Cord of the Lamprey

Development and neuromodulation of spinal locomotor networks in the metamorphosing frog

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