Adrenoreceptor‐mediated modulation of the spinal locomotor pattern during swimming in <i>Xenopus laevis</i> tadpoles

Fischer, Hanno; Merrywest, Simon D.; Sillar, Keith T.

doi:10.1046/j.1460-9568.2001.01468.x

Cited by 15 publications

(32 citation statements)

References 55 publications

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“…NA has three modulatory effects on fictive swimming: (1) it also slows swimming frequency by increasing glycinergic inhibition from commissural interneurons (McDearmid et al, 1997); (2) it can increase GABA release onto motor neurons, shortening swimming episode durations (McDearmid, 1998;Fischer et al, 2001); and (3) it can decrease the longitudinal delay of motor bursts along the body by enhancing postinhibitory rebound in motor neurons (Merrywest et al, 2003). NA mediates these three effects via the activation of ␣-adrenoreceptors (Fischer et al, 2001;Merrywest et al, 2002Merrywest et al, , 2003. Because of these similarities in both the effects on swimming and the underlying mechanisms, we used two pharmacological strategies to investigate the possible hierarchical relationship between NO and NA.…”

Section: Resultsmentioning

confidence: 99%

Metamodulation of a Spinal Locomotor Network by Nitric Oxide

McLean

Sillar

2004

J. Neurosci.

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Flexibility in the output of spinal networks can be accomplished by the actions of neuromodulators; however, little is known about how the process of neuromodulation itself may be modulated. Here we investigate the potential "meta"-modulatory hierarchy between nitric oxide (NO) and noradrenaline (NA) in Xenopus laevis tadpoles. NO and NA have similar effects on fictive swimming; both potentiate glycinergic inhibition to slow swimming frequency and GABAergic inhibition to reduce episode durations. In addition, both modulators have direct effects on the membrane properties of motor neurons. Here we report that antagonism of noradrenergic pathways with phentolamine dramatically influences the effect of the NO donor S-nitroso-N-acetylpenicillamine (SNAP) on swimming frequency, but not its effect on episode durations. In contrast, scavenging extracellular NO with 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (PTIO) does not influence any of the effects of NA on fictive swimming. These data place NO above NA in the metamodulatory hierarchy, strongly suggesting that NO works via a noradrenergic pathway to control glycine release but directly promotes GABA release. We confirmed this possibility using intracellular recordings from motor neurons. In support of a natural role for NO in the Xenopus locomotor network, PTIO not only antagonized all of the effects of SNAP on swimming but also, when applied on its own, modulated both swimming frequency and episode durations in addition to the underlying glycinergic and GABAergic pathways. Collectively, our results illustrate that NO and NA have parallel effects on motor neuron membrane properties and GABAergic inhibition, but that NO serially metamodulates glycinergic inhibition via NA.

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Section: Resultsmentioning

confidence: 99%

Metamodulation of a Spinal Locomotor Network by Nitric Oxide

McLean

Sillar

2004

J. Neurosci.

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“…Numerous studies have emphasized the role of the NAergic system in motor rhythms and segmental reflex modulations in animal models and humans (as for examples: Kitazawa et al, 1985; Chau et al, 1998a; Jankowska et al, 1998; Kiehn et al, 1999; Remy-Neris et al, 1999; Sqalli-Houssaini and Cazalets, 2000; Fischer et al, 2001; Barbeau and Norman, 2003; Gabbay and Lev-Tov, 2004; Machacek and Hochman, 2006; Barriere et al, 2008). Our data shed light on the complexity of the cellular bases of the NAergic modulation in the motor spinal networks.…”

Section: Discussionmentioning

confidence: 99%

Noradrenergic modulation of intrinsic and synaptic properties of lumbar motoneurons in the neonatal rat spinal cord

Tartas

Barrière

Goillandeau

et al. 2010

Front. Neural Circuits

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Although it is known that noradrenaline (NA) powerfully controls spinal motor networks, few data are available regarding the noradrenergic (NAergic) modulation of intrinsic and synaptic properties of neurons in motor networks. Our work explores the cellular basis of NAergic modulation in the rat motor spinal cord. We first show that lumbar motoneurons express the three classes of adrenergic receptors at birth. Using patch-clamp recordings in the newborn rat spinal cord preparation, we characterized the effects of NA and of specific agonists of the three classes of adrenoreceptors on motoneuron membrane properties. NA increases the motoneuron excitability partly via the inhibition of a KIR like current. Methoxamine (α1), clonidine (α2) and isoproterenol (β) differentially modulate the motoneuron membrane potential but also increase motoneuron excitability, these effects being respectively inhibited by the antagonists prazosin (α1), yohimbine (α2) and propranolol (β). We show that the glutamatergic synaptic drive arising from the T13-L2 network is enhanced in motoneurons by NA, methoxamine and isoproterenol. On the other hand, NA, isoproterenol and clonidine inhibit both the frequency and amplitude of miniature glutamatergic EPSCs while methoxamine increases their frequency. The T13-L2 synaptic drive is thereby differentially modulated from the other glutamatergic synapses converging onto motoneurons and enhanced by presynaptic α1 and β receptor activation. Our data thus show that the NAergic system exerts a powerful and complex neuromodulation of lumbar motor networks in the neonatal rat spinal cord.

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“…It has recently been shown that noradrenergic modulation of the spinal swim‐pattern generator in Xenopus may be mediated via activation of α‐ and β‐adrenoreceptors. Both α 1 ‐ and α 2 ‐receptors modulate the frequency and duration of swimming, while α 1 ‐ and β‐receptors modulate longitudinal co‐ordination (Fischer et al ., 2001).…”

Section: Introductionmentioning

confidence: 99%

Alpha‐adrenoreceptor activation modulates swimming via glycinergic and GABAergic inhibitory pathways in Xenopus laevis tadpoles

Merrywest

Fischer

Sillar

2002

Eur J of Neuroscience

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This study focuses upon the network pathways underlying the adrenoreceptor-mediated modulation of fictive swimming in the immobilized Xenopus laevis tadpole. As shown recently, noradrenaline (NA) increases cycle periods while simultaneously reducing the rostrocaudal delay in head-to-tail firing and the duration of swimming episodes. Furthermore, both swimming frequency and duration are reduced by selective pharmacological activation of alpha1- and/or alpha2-adrenoreceptors, while alpha1-receptor activation also reduces rostrocaudal delays. We show that NA could still modulate aspects of swimming after blocking either glycine or GABA(A) receptors with strychnine and bicuculline, respectively. Furthermore, after prior application of NA, strychnine could counteract noradrenergic effects on cycle periods and rostrocaudal delays, while bicuculline could counteract effects on cycle periods, suggesting that these two fast inhibitory pathways are both involved in the NA modulation of swimming. In addition, blocking glycine receptors reduced the effects of alpha1-receptors on cycle periods and delays, while blocking GABA(A) receptors had no effect. Blocking either glycine or GABA(A) receptors, however, lessened the reduction in swimming frequency by alpha2-receptors. In addition, pre-application of bicuculline prevented a reduction in episode durations by NA, alpha1- and alpha2-receptors. Our findings suggest that the noradrenergic modulation of Xenopus swimming is mediated via alpha-adrenoreceptors interacting with both glycinergic and GABAergic inhibitory pathways. Both alpha1- and alpha2-receptor activation influences the GABAergic pathway controlling the duration of swimming episodes and is involved in the glycinergic modulation of the swimming rhythm and its longitudinal co-ordination, with alpha2-receptors additionally affecting swimming frequency through GABAergic pathways.

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Adrenoreceptor‐mediated modulation of the spinal locomotor pattern during swimming in Xenopus laevis tadpoles

Cited by 15 publications

References 55 publications

Metamodulation of a Spinal Locomotor Network by Nitric Oxide

Metamodulation of a Spinal Locomotor Network by Nitric Oxide

Noradrenergic modulation of intrinsic and synaptic properties of lumbar motoneurons in the neonatal rat spinal cord

Alpha‐adrenoreceptor activation modulates swimming via glycinergic and GABAergic inhibitory pathways in Xenopus laevis tadpoles

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