Neuromodulation and developmental plasticity in the locomotor system of anuran amphibians during metamorphosis

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

doi:10.1016/j.brainresrev.2007.07.018

Cited by 50 publications

(40 citation statements)

References 37 publications

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“…Given the strong similarities in the mechanisms that regulate diverse rhythmic motor behaviours, the developmental changes in locomotion that take place during Xenopus metamorphosis can provide valuables cues in this regard. For instance, exogenous nitric oxide (NO) application facilitates locomotor activity in adult frogs, an effect that contrasts with the inhibition of swimming at earlier larval stages (Sillar et al, 2008). But in the present context, it is interesting to note that NO modulates swimming by facilitating the release of GABA and glycine (Sillar et al, 2008).…”

Section: Conclusion and Perspectivementioning

confidence: 85%

Corticosterone promotes emergence of fictive air breathing in Xenopus laevis Daudin tadpole brainstems

Fournier

Dubé

Kinkead

2012

Journal of Experimental Biology

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SUMMARY The emergence of air breathing during amphibian metamorphosis requires significant changes to the brainstem circuits that generate and regulate breathing. However, the mechanisms controlling this developmental process are unknown. Because corticosterone plays an important role in the neuroendocrine regulation of amphibian metamorphosis, we tested the hypothesis that corticosterone augments fictive air breathing frequency in Xenopus laevis. To do so, we compared the fictive air breathing frequency produced by in vitro brainstem preparations from pre-metamorphic tadpoles and adult frogs before and after 1 h application of corticosterone (100 nmol l–1). Fictive breathing measurements related to gill and lung ventilation were recorded extracellularly from cranial nerve rootlets V and X. Corticosterone application had no immediate effect on respiratory-related motor output produced by brainstems from either developmental stage. One hour after corticosterone wash out, fictive lung ventilation frequency was increased whereas gill burst frequency was decreased. This effect was stage specific as it was significant only in preparations from tadpoles. GABA application (0.001–0.5 mmol l–1) augmented fictive air breathing in tadpole preparations. However, this effect of GABA was no longer observed following corticosterone treatment. An increase in circulating corticosterone is one of the endocrine processes that orchestrate central nervous system remodelling during metamorphosis. The age-specific effects of corticosterone application indicate that this hormone can act as an important regulator of respiratory control development in Xenopus tadpoles. Concurrent changes in GABAergic neurotransmission probably contribute to this maturation process, leading to the emergence of air breathing in this species.

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Section: Conclusion and Perspectivementioning

confidence: 85%

Corticosterone promotes emergence of fictive air breathing in Xenopus laevis Daudin tadpole brainstems

Fournier

Dubé

Kinkead

2012

Journal of Experimental Biology

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“…R. Soc. B 371: 20150057 metamorphosis offers a glimpse into how the evolutionary process of transforming a CPG based on an axial half-centre to a limb-based locomotor system might have occurred [20][21][22]. Tadpoles swim by progressive undulations of their tail (figure 3a), with the left and right sides in alternation at any time.…”

Section: Divergence Of Central Pattern Generators and Rhythmic Behavimentioning

confidence: 99%

Evolution of central pattern generators and rhythmic behaviours

Katz

2016

Phil. Trans. R. Soc. B

165

126

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One contribution of 16 to a discussion meeting issue 'Homology and convergence in nervous system evolution'. Comparisons of rhythmic movements and the central pattern generators (CPGs) that control them uncover principles about the evolution of behaviour and neural circuits. Over the course of evolutionary history, gradual evolution of behaviours and their neural circuitry within any lineage of animals has been a predominant occurrence. Small changes in gene regulation can lead to divergence of circuit organization and corresponding changes in behaviour. However, some behavioural divergence has resulted from large-scale rewiring of the neural network. Divergence of CPG circuits has also occurred without a corresponding change in behaviour. When analogous rhythmic behaviours have evolved independently, it has generally been with different neural mechanisms. Repeated evolution of particular rhythmic behaviours has occurred within some lineages due to parallel evolution or latent CPGs. Particular motor pattern generating mechanisms have also evolved independently in separate lineages. The evolution of CPGs and rhythmic behaviours shows that although most behaviours and neural circuits are highly conserved, the nature of the behaviour does not dictate the neural mechanism and that the presence of homologous neural components does not determine the behaviour. This suggests that although behaviour is generated by neural circuits, natural selection can act separately on these two levels of biological organization.

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“…In contrast, escape behaviour in most species of birds uniquely transitions from obligatory terrestrial bipedalism in juveniles to flight in adults. Only amphibians undergo similar dramatic ontogenetic shifts in locomotor strategies (Sillar et al 2008). Compared with the two-way trade-off associated with most developing animals (i.e.…”

Section: Introductionmentioning

confidence: 99%

Precocial development of locomotor performance in a ground-dwelling bird (Alectoris chukar): negotiating a three-dimensional terrestrial environment

2009

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Developing animals are particularly vulnerable to predation. Hence, precocial young of many taxa develop predator escape performance that rivals that of adults. Ontogenetically unique among vertebrates, birds transition from hind limb to forelimb dependence for escape behaviours, so developmental investment for immediate gains in running performance may impair flight performance later. Here, in a three-dimensional kinematic study of developing birds performing pre-flight flapping locomotor behaviours, wing-assisted incline running (WAIR) and a newly described behaviour, controlled flapping descent (CFD), we define three stages of locomotor ontogeny in a model gallinaceous bird (Alectoris chukar). In stage I (1 -7 days post-hatching (dph)) birds crawl quadrupedally during ascents, and their flapping fails to reduce their acceleration during aerial descents. Stage II (8 -19 dph) birds use symmetric wing beats during WAIR, and in CFD significantly reduce acceleration while controlling body pitch to land on their feet. In stage III (20 dph to adults), birds are capable of vertical WAIR and level-powered flight. In contrast to altricial species, which first fly when nearly at adult mass, we show that in a precocial bird the major requirements for flight (i.e. high power output, wing control and wing size) convene by around 8 dph (at ca 5% of adult mass) and yield significant gains in escape performance: immature chukars can fly by 20 dph, at only about 12 per cent of adult mass.

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Neuromodulation and developmental plasticity in the locomotor system of anuran amphibians during metamorphosis

Cited by 50 publications

References 37 publications

Corticosterone promotes emergence of fictive air breathing in Xenopus laevis Daudin tadpole brainstems

Corticosterone promotes emergence of fictive air breathing in Xenopus laevis Daudin tadpole brainstems

Evolution of central pattern generators and rhythmic behaviours

Precocial development of locomotor performance in a ground-dwelling bird (Alectoris chukar): negotiating a three-dimensional terrestrial environment

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