Sites of respiratory rhythmogenesis during development in the tadpole

Torgerson, C. S.; Gdovin, Matthew J.; Remmers, John E.

doi:10.1152/ajpregu.2001.280.4.r913

Cited by 30 publications

(31 citation statements)

References 28 publications

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“…In line with this, morphological studies in marine toads suggested that the major sources of trigeminal input are the muscle spindles in the jaw-tongue coordination (Mandal and Anderson, 2010). As the facial motoneurons are involved in other behaviors like vomiting, respiration, vocalization (Schmidt, 1966;Broch et al, 2002;Torgerson et al, 2001;Liao et al, 1996;Martin and Gans, 1972) the direct trigeminal input described here may contribute to the rapid modification of these motor programs.…”

Section: Discussionsupporting

confidence: 62%

Possible neural network mediating jaw opening during prey-catching behavior of the frog

Kovalecz

Kecskes

Birinyi

et al. 2015

Brain Research Bulletin

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Please cite this article in press as: Kovalecz, G., et al., Termination of trigeminal afferent fibers on facial motoneurons: Possible neural network mediating jaw opening during prey-catching behavior of the frog. Brain Res. Bull. (2015) a b s t r a c tThe prey-catching behavior of the frog is a complex, well-timed sequence of stimulus response chain of movements. After visual analysis of the prey, a size dependent program is selected in the motor pattern generator of the brainstem. Besides this predetermined feeding program, various direct and indirect sensory inputs provide flexible adjustment for the optimal contraction of the executive muscles. The aim of the present study was to investigate whether trigeminal primary afferents establish direct contacts with the jaw opening motoneurons innervated by the facial nerve. The experiments were carried out on Rana esculenta (Pelophylax esculentus), where the trigeminal and facial nerves were labeled simultaneously with different fluorescent dyes. Using a confocal laser scanning microscope, close appositions were detected between trigeminal afferent fibers and somatodendritic components of the facial motoneurons.Quantitative analysis revealed that the majority of close contacts were encountered on the dendrites of facial motoneurons and approximately 10% of them were located on the perikarya. We suggest that the identified contacts between the trigeminal afferents and facial motoneurons presented here may be one of the morphological substrate in the feedback and feedforward modulation of the rapidly changing activity of the jaw opening muscle during the prey-catching behavior.

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Section: Discussionsupporting

confidence: 62%

Possible neural network mediating jaw opening during prey-catching behavior of the frog

Kovalecz

Kecskes

Birinyi

et al. 2015

Brain Research Bulletin

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“…During decerebration and subsequent dissection, the brainstem was constantly perfused with cold (5-10°C) artificial cerebrospinal fluid (aCSF) with the following composition: (in mmol·l Torgerson et al, 2001).…”

Section: Methodsmentioning

confidence: 99%

Development of the respiratory response to hypoxia in the isolated brainstem of the bullfrogRana catesbeiana

Winmill

Chen

Hedrick

2005

Journal of Experimental Biology

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SUMMARY The aim of this study was to examine the effects of cellular hypoxia, and the contribution of anaerobic metabolism, on respiratory activity in bullfrogs at different stages of development. Respiratory-related neural activity was recorded from cranial nerve rootlets in isolated brainstem preparations from pre-metamorphic (Taylor–Köllros (T-K) stages VIII-XVI) and postmetamorphic tadpoles (T-K stages XXIV-XXV) and adults. Changes in fictive gill/lung activity in brainstems from pre-metamorphic tadpoles and lung activity in postmetamorphic tadpoles and adults were examined during superfusion with control (98% O2/2% CO2) or hypoxic (98%N2/2% CO2) artificial cerebrospinal fluid (aCSF). Iodoacetate (IAA; 100 μmol l–1) was used in conjunction with hypoxic aCSF to inhibit glycolysis. Gill burst frequency in pre-metamorphic brainstems did not change over a 3 h exposure to hypoxia and fictive lung burst frequency slowed significantly, but only after 3 h hypoxia. Blockade of glycolysis with IAA during hypoxia significantly reduced the time respiratory activity could be maintained in pre-metamorphic, but not in adult,brainstems. In brainstems from post-metamorphic tadpoles and adults, lung burst frequency became significantly more episodic within 5–15 min hypoxic exposure, but respiratory neural activity was subsequently abolished in every preparation. The cessation of fictive breathing was restored to control levels upon reoxygenation. Neither tadpole nor adult brainstems exhibited changes in neural bursts resembling `gasping' that is observed in mammalian brainstems exposed to severe hypoxia. There was also a significant increase in the frequency of `non-respiratory' bursts in hypoxic postmetamorphic and adult brainstems, but not in pre-metamorphic brainstems. These results indicate that pre-metamorphic tadpoles are capable of maintaining respiratory activity for 3 h or more during severe hypoxia and rely to a great extent upon anaerobic metabolism to maintain respiratory motor output. Upon metamorphosis, however, hypoxia results in significant changes in respiratory frequency and pattern, including increased lung burst episodes,non-ventilatory bursts and a reversible cessation of respiratory activity. Adults have little or no ability to maintain respiratory activity through glycolysis but, instead, stop respiratory activity until oxygen is available. This `switch' in the respiratory response to hypoxia coincides morphologically with the loss of gills and obligate air-breathing in the postmetamorphic frog. We hypothesize that the cessation of respiratory activity in post-metamorphic tadpoles and adults is an adaptive, energy-saving response to low oxygen.

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“…(35) Consistent with a functional difference between gill and lung CPGs, microinjections of AMPA and GABA in the tadpole brainstem identified two distinct neuronal oscillators (36) that were anatomically separable. (36,37) Phylogenetic conservation of respiratory rhythm generators Following metamorphosis in tadpoles, the gills degenerate and the frog breathes air exclusively. However, a gill ventilationlike rhythm persists in the adult as oscillations of the buccal cavity that go on between runs of lung breaths.…”

Section: Ancestral Ventilationmentioning

confidence: 99%

A phylogenetic hypothesis for the origin of hiccough

et al. 2003

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The occurrence of hiccoughs (hiccups) is very widespread and yet their neuronal origin and physiological significance are still unresolved. Several hypotheses have been proposed. Here we consider a phylogenetic perspective, starting from the concept that the ventilatory central pattern generator of lower vertebrates provides the base upon which central pattern generators of higher vertebrates develop. Hiccoughs are characterized by glottal closure during inspiration and by early development in relation to lung ventilation. They are inhibited when the concentration of inhaled CO(2) is increased and they can be abolished by the drug baclofen (an agonist of the GABA(B) receptor). These properties are shared by ventilatory motor patterns of lower vertebrates, leading to the hypothesis that hiccough is the expression of archaic motor patterns and particularly the motor pattern of gill ventilation in bimodal breathers such as most frogs. A circuit that can generate hiccoughs may persist in mammals because it has permitted the development of pattern generators for other useful functions of the pharynx and chest wall muscles, such as suckling or eupneic breathing.

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Sites of respiratory rhythmogenesis during development in the tadpole

Cited by 30 publications

References 28 publications

Possible neural network mediating jaw opening during prey-catching behavior of the frog

Possible neural network mediating jaw opening during prey-catching behavior of the frog

Development of the respiratory response to hypoxia in the isolated brainstem of the bullfrogRana catesbeiana

A phylogenetic hypothesis for the origin of hiccough

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