Mechanisms and significance of reduced activity and responsiveness in resting frog tadpoles

Lambert, Thomas D.; Howard, Jenny; Plant, Andy; Soffe, Stephen R; Roberts, Alan

doi:10.1242/jeb.00866

Cited by 18 publications

(25 citation statements)

References 52 publications

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“…Related to this issue, a recent study has investigated the potential involvement of NO in the mid-hindbrain reticulospinalmediated stopping response in Xenopus embryos (Lambert et al, 2004). At this early stage in development, they failed to find a prominent role for NO in this pathway using NO synthase inhibitors, which is consistent with the notion that an endogenous role for NO in mediating GABA release does not appear reliably until larval stages.…”

Section: Modulation Of Descending Systems By Nitric Oxidementioning

confidence: 69%

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: Modulation Of Descending Systems By Nitric Oxidementioning

confidence: 69%

Metamodulation of a Spinal Locomotor Network by Nitric Oxide

McLean

Sillar

2004

J. Neurosci.

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“…The methods for making recordings from the motor nerves have been described previously (e.g. Lambert et al, 2004). Briefly, tadpoles were anaesthetised with 0.1% MS-222 in saline for 20-30 s, then pinned onto a rotatable Sylgard block in a bath of saline.…”

Section: Electrophysiologymentioning

confidence: 99%

“…Each tadpole was tested once. We checked that they were not attached to the bottom of the dish by cement from their cement gland since this inhibits responses (Lambert et al, 2004). We first evaluated spontaneous swimming in unstimulated tadpoles.…”

Section: Basic Swimming Responses To Water Currentsmentioning

confidence: 99%

Responses of hatchlingXenopustadpoles to water currents: first function of lateral line receptors without cupulae

Roberts

Feetham

Pajak

et al. 2009

Journal of Experimental Biology

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SUMMARYAt later stages in larval life and also as adults, Xenopus can respond to water currents detected by their lateral-line sensory system. We have investigated when responses to water currents first appear and whether the first lateral line neuromasts operate in the same way as the adult organs. Just before and after hatching from their egg membranes we show that Xenopus embryos and tadpoles can respond to water currents by swimming into them. Local stimulation in immobilised animals where motor activity was recorded electrically suggested that the receptors detecting water currents were located between the eyes and the gills and were innervated by cranial nerves. In behaving tadpoles, responses to water currents were reduced following skin abrasion caudal to the eyes or treatment with neomycin, which is known to block hair cell function. We therefore used scanning electron microscopy to establish that rows of lateral line neuromasts with hair cells and kinocilia are present just caudal to the eyes at these stages of development. However, careful observations and manipulations of the kinocilia of neuromasts in living tadpoles failed to find any evidence that kinocilia were embedded in a jelly-like cupula. We conclude that, when they first start to function, these early neuromasts detect water movements which directly move their freely exposed hair cell kinocilia projecting out from the skin surface. Possible behavioural roles for the tadpoles responses to water are discussed.

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“…This unique behavior depends on the mandibular branch of trigeminal sensory nerve that senses the attachment state of the embryos and suppresses muscle movement (Lambert et al 2004). A recent study showed that brain-derived neurotrophic factor secreted from the cement gland could provide a short-range attractive guidance signal that stimulates axon arborization and growth into the cement gland (Huang et al 2007).…”

Section: Resultsmentioning

confidence: 99%

“…They form an ophthalmic and a mandibular branch, and the latter has a transient pathway that innervates the embryonic cement gland (Roberts and Clarke 1982;Jacobson and Huang 1985). This branch has been shown to regulate attachmentdependent suppression of the embryo's swimming behavior (Lambert et al 2004).…”

Section: Introductionmentioning

confidence: 99%

Contactin 1 knockdown in the hindbrain induces abnormal development of the trigeminal sensory nerve in Xenopus embryos

Fujita

Nagata

2007

Dev Genes Evol

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In Xenopus tailbud embryos, the mandibular branch of trigeminal sensory nerve has a transient pathway innervating the cement gland. This pathway is settled by pioneer neurons in the trigeminal ganglion and along which extend later-growing axons from the trigeminal ganglion and the hindbrain. Axons in this branch express a neuronal recognition molecule, Contactin 1, from the initial stage of its outgrowth in early tailbud embryos and form a tightly joined, strongly Contactin 1-positive fascicle in the later stages. When the expression vector encoding the enhanced green fluorescent protein was electrotransfected into the brain neurons of early tailbud embryos, the fluorescence was detected in the hindbrain and the trigeminal nerve at late tailbud stages. Cotransfection of antisense vector caused knockdown of Contactin 1 concurrent with defasciculation and misguidance of the sensory axons in the trigeminal mandibular branch. The results suggest that Contactin 1 is required for the growing axon of hindbrain sensory neurons to recognize and follow the pathway settled by the pioneer neurons.

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Mechanisms and significance of reduced activity and responsiveness in resting frog tadpoles

Cited by 18 publications

References 52 publications

Metamodulation of a Spinal Locomotor Network by Nitric Oxide

Metamodulation of a Spinal Locomotor Network by Nitric Oxide

Responses of hatchlingXenopustadpoles to water currents: first function of lateral line receptors without cupulae

Contactin 1 knockdown in the hindbrain induces abnormal development of the trigeminal sensory nerve in Xenopus embryos

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