Metamorphosis in anuran amphibians requires a complete transformation in locomotor strategy from undulatory tadpole swimming to adult quadrupedal propulsion. The underlying reconfiguration of spinal networks may be influenced by various neuromodulators including nitric oxide, which is known to play an important role in CNS development and plasticity in diverse species, including metamorphosis of amphibians. Using NADPH-diaphorase (NADPH-d) staining and neuronal nitric oxide synthase (nNOS) immunofluorescence labelling, the expression and developmental distribution of NOS-containing neurons in the spinal cord and brainstem were analysed in all metamorphic stages of Xenopus laevis. Wholemount preparations of the spinal cord from early stages of metamorphosis (coincident with emergence of the fore- and hindlimb buds) revealed two clusters of NOS-positive neurons interspersed with areas devoid of stained somata. These cells were distributed in three topographic subgroups, the most ventral of which had axonal projections that crossed the ventral commissure. Motoneurons innervating the fore- and hindlimb buds were retrogradely labelled with horseradish peroxidase (HRP) to determine their position in relation to the two NOS-expressing cord regions. Limb motoneurons and NOS-positive cells did not overlap, indicating that during early stages of metamorphosis nitrergic neurons are excluded from regions where spinal limb circuits are forming. As metamorphosis progresses, NOS expression became distributed along the length of the spinal cord together with an increase in the number and intensity of labelled cells and fibers. NOS expression reached a peak as the forelimbs emerge then declined. These findings are consistent with a role for nitric oxide (NO) in the developmental transition from undulatory swimming to quadrupedal locomotion.
The skin is the main interface between the external environment and internal body structures of an organism and as such represents a strategic point of defense. Typically, the skin is a passive structure that acts as a protective barrier, and lacks a means of direct communication between constituent cells. However, the skin of many amphibian tadpoles functions as a sensory system in its own right. For a brief period from midembryonic until early larval development, cells of the tadpole skin exhibit properties of nervous tissue when presented with a noxious stimulus anywhere on their surface (reviewed in Roberts, 1998). This excitability takes the form of an action potential or 'skin impulse,' which resembles a cardiac action potential in duration and waveform, and propagates from the point of initiation throughout the skin via electrical connections between neighbouring cells. A range of anurans, including the South African clawed frog Xenopus laevis (Daudin), the common frog Rana temporaria, the common toad Bufo bufo, and salamanders such as Amystoma, have been shown to display such excitability (Roberts, 1998). One known function of the skin impulse is to trigger escape behaviour and thereby allow the tadpole to evade predation.In Xenopus, the skin impulse pathway is one of two sensory systems in the skin that operate in parallel (Roberts and Smyth, 1974), the second one involving a more conventional innervation by mechanosensory Rohon-Beard (R-B) cells, a subset of extra-ganglionic sensory neurones (Hughes, 1957). In early embryos, at stage 27 [about 24·h post-fertilization (Nieuwkoop and Faber, 1956)], the skin is already excitable, including in areas yet to be innervated by R-B cells. Both the skin impulse and the R-B cells can activate neural circuitry of the spinal cord to initiate trunk flexion in young embryos and rhythmic swimming movements in older embryos and larvae, but through different routes. R-B cells directly activate spinal neurons (Clarke et al., 1984;Sillar and Roberts, 1988), while the skin impulse appears to gain access to the central nervous system (CNS) via a branch of the trigeminal nerve, bypassing primary sensory R-B neurons in the skin (Roberts, 1996). Thus the electrically excitable epithelium functions as a bona fide sensory system, which initially precedes and then operates in parallel with more conventional mechanosensory innervation, before its excitable properties disappear during later larval life.Most cutaneous sensory systems are subject to modification under different circumstances (Sillar, 1989). The presence of a range of neuromodulatory substances in the skin of Xenopus raises the possibility that the skin impulse and its propagation through the epithelium may be subject to regulation, as is the case for other, more conventional sensory systems. One such modulator, which is produced by the skin of many vertebrates, including humans (Weller, 1997), is the free radical, nitric oxide (NO). NADPH-diaphorase labeling, a marker for the presence of the NO synthetic enzyme NOS, ...
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