scholarly journals Orexin-A inhibits fictive air breathing responses to respiratory stimuli in the bullfrog tadpole (Lithobates catesbeianus)

2021 ◽  
Vol 224 (8) ◽  
Author(s):  
Elisa M. Fonseca ◽  
Tara A. Janes ◽  
Stéphanie Fournier ◽  
Luciane H. Gargaglioni ◽  
Richard Kinkead

ABSTRACT In pre-metamorphic tadpoles, the neural network generating lung ventilation is present but actively inhibited; the mechanisms leading to the onset of air breathing are not well understood. Orexin (ORX) is a hypothalamic neuropeptide that regulates several homeostatic functions, including breathing. While ORX has limited effects on breathing at rest, it potentiates reflexive responses to respiratory stimuli mainly via ORX receptor 1 (OX1R). Here, we tested the hypothesis that OX1Rs facilitate the expression of the motor command associated with air breathing in pre-metamorphic bullfrog tadpoles (Lithobates catesbeianus). To do so, we used an isolated diencephalic brainstem preparation to determine the contributions of OX1Rs to respiratory motor output during baseline breathing, hypercapnia and hypoxia. A selective OX1R antagonist (SB-334867; 5–25 µmol l−1) or agonist (ORX-A; 200 nmol l−1 to 1 µmol l−1) was added to the superfusion media. Experiments were performed under basal conditions (media equilibrated with 98.2% O2 and 1.8% CO2), hypercapnia (5% CO2) or hypoxia (5–7% O2). Under resting conditions gill, but not lung, motor output was enhanced by the OX1R antagonist and ORX-A. Hypercapnia alone did not stimulate respiratory motor output, but its combination with SB-334867 increased lung burst frequency and amplitude, lung burst episodes, and the number of bursts per episode. Hypoxia alone increased lung burst frequency and its combination with SB-334867 enhanced this effect. Inactivation of OX1Rs during hypoxia also increased gill burst amplitude, but not frequency. In contrast with our initial hypothesis, we conclude that ORX neurons provide inhibitory modulation of the CO2 and O2 chemoreflexes in pre-metamorphic tadpoles.


2002 ◽  
Vol 93 (3) ◽  
pp. 936-946 ◽  
Author(s):  
Richard Kinkead ◽  
Olivier Belzile ◽  
Roumiana Gulemetova

To test the hypothesis that serotonin (5-hydroxytryptamine; 5-HT)-receptor activation elicits age-dependent changes in respiratory motor output, we compared the effects of 5-HT bath application (5-HT concentration = 0.5–25 μM) onto in vitro brain stem preparations from pre- and postmetamorphic bullfrog tadpoles. Recording of motor output related to gill and lung ventilation showed that 5-HT elicits a dose-dependent depression of gill burst frequency in both groups. In contrast, the lung burst frequency response was stage dependent; an increase in lung burst frequency at low 5-HT concentration (≤0.5 μM) was observed only in the postmetamorphic group. Higher 5-HT concentrations decreased lung burst frequency in all preparations. Gill burst frequency attenuation is mediated (at least in part) by 5-HT1A-receptor activation in an age-dependent fashion. We conclude that serotonergic modulation of respiratory motor output 1) changes during tadpole development and 2) is distinct for gill and lung ventilation.



1994 ◽  
Vol 77 (4) ◽  
pp. 2048-2051 ◽  
Author(s):  
R. Kinkead ◽  
W. G. Filmyer ◽  
G. S. Mitchell ◽  
W. K. Milsom

This study investigated the interaction between vagal afferent input and central chemosensitivity in modulating the respiratory motor output of in vitro brain stem-spinal cord preparations from adult bullfrogs. With this preparation, the spatiotemporal distribution of respiratory-related motor output emulated that of intact bullfrogs; that is, the fictive breathing pattern was mostly episodic. Recordings from cranial motor nerves (V and X) showed that, without peripheral feedback, increasing the PCO2 of the mock cerebrospinal fluid (thereby reducing pH from 8.3 to 7.7) caused a modest increase in respiration-related burst frequency. When the pulmonary branch of a vagus nerve was stimulated phasically (2 V, 20 Hz, 0.2 ms) during each fictive breath to simulate afferent pulmonary stretch receptor feedback 1) the responsiveness of the preparation to the same changes in pH was augmented nearly threefold and 2) the breathing pattern remained episodic. It appears, therefore, that episodic breathing is an intrinsic property of the central nervous system in bullfrogs. It is concluded that there is a strong interaction between vagal feedback and central chemodetection in controlling the temporal relationships that characterize this episodic breathing pattern.



1992 ◽  
Vol 263 (3) ◽  
pp. R602-R608
Author(s):  
W. W. Burggren ◽  
J. E. Bicudo ◽  
M. L. Glass ◽  
A. S. Abe

Systemic arterial blood pressure and heart rate (fH) were measured in unanesthetized, unrestrained larvae and adults of the paradoxical frog, Pseudis paradoxus from Sao Paulo State in Brazil. Four developmental groups were used, representing the complete transition from aquatic larvae to primarily air-breathing adults. fH (49-66 beats/min) was not significantly affected by development, whereas mean arterial blood pressure was strongly affected, being lowest in the stage 37-39 larvae (10 mmHg), intermediate in the stage 44-45 larvae (18 mmHg), and highest in the juveniles and adults (31 and 30 mmHg, respectively). Blood pressure was not significantly correlated with body mass, which was greatest in the youngest larvae and smallest in the juveniles. In the youngest larvae studied (stages 37-39), lung ventilation was infrequent, causing a slight decrease in arterial blood pressure but no change in heart rate. Lung ventilation was more frequent in stages 44-45 larvae and nearly continuous in juveniles and adults floating at the surface. Bradycardia during both forced and voluntary diving was observed in almost every advanced larva, juvenile, and adult but in only one of four young larvae. Developmentally related changes in blood pressure were not complete until metamorphosis, whereas diving bradycardia was present at an earlier stage.



1988 ◽  
Vol 66 (1) ◽  
pp. 109-123 ◽  
Author(s):  
G. Shelton ◽  
P. C. Croghan

Control of breathing and gas exchange has been extensively investigated in unimodal animals, particularly mammals, in which ventilation is characteristically a regular and continuous process and gas exchange approximates to a steady-state system. Both static and dynamic models have been developed in control-theory analyses. Similar analyses are possible in unimodal fish, though few have been carried out. Control in bimodal animals, such as air-breathing fish and amphibians, is more difficult to understand and model. The evolutionary change from water to air breathing in vertebrates involves not only the adjustment of many control processes but also the development, in the early stages, of non steady states in gas exchangers, blood, and tissues. A simple control-system model, differing from mammalian counterparts in its greater emphasis on storage functions and its intermittently activated controller, is described for two suggested stages in the evolution of air breathing. The first of these stages is air gulping, in which a fixed and rather brief pattern of air breathing is activated by internal signals generated as a result of the inadequacy of the gills to provide sufficient oxygen for tissue metabolism. The second stage is that of burst breathing, in which lung ventilation is both begun and ended by internal signals so that burst duration is variable. The effects of adjusting parameters on variables of evolutionary importance, such as dive duration, burst duration, store renewal, and metabolic rate, can be examined in these two versions of the model. Refinements to incorporate arterial and venous compartments in the circulatory system, the shunting of venous and arterial blood streams in the heart, realistic oxygen dissociation curves, controller inputs from a wider range of sources, and the capacity to respond to some conditions with changes in ventilation rate as well as in burst and dive durations, are being developed. They should make the complex, non-steady-state interactions between gas exchangers, circulating blood, and tissues easier to understand and indicate the likely steps toward the evolution of steady-state systems seen in birds and mammals.



Paleobiology ◽  
2016 ◽  
Vol 42 (2) ◽  
pp. 289-304 ◽  
Author(s):  
A. M. Clement ◽  
J. A. Long ◽  
P. Tafforeau ◽  
P. E. Ahlberg

AbstractLungfishes are known for, and indeed take their name from, their bimodal respiratory abilities. All three extant genera can use their lungs to extract oxygen from the atmosphere, although their reliance upon this capability differs among taxa. Lungs are considered primitive for the Osteichthyes, however the distinctive buccal pump mode of air gulping exhibited by extant lungfishes appears to be a specialization. It is associated with a number of derived skeletal characters (cranial ribs, long parasphenoid stalk, midline gap between palatal tooth plates) that first appeared during the Devonian. These have been described individually, but in no Devonian lungfish has their three-dimensional (3D) spatial relationship been reconstructed and analyzed. Here we present the 3D morphology of Rhinodipterus, a Mid-Late Devonian lungfish from Australia and Europe, based on synchrotron tomography and conventional microtomography scans.Unlike less crownward contemporaneous lungfishes such as Griphognathus and Chirodipterus, Rhinodipterus has a full set of skeletal buccal pump components that can be directly compared to those of extant lungfishes, suggesting that it made more extensive use of air breathing than other Gogo or Bergisch Gladbach genera. This is interesting in relation to the environmental context as Gogo and Bergisch Gladbach are both marine, contrasting with the frequently hypoxic tropical to subtropical fresh water environments inhabited by modern lungfishes. The evolution of buccal pump-supported lung ventilation was evidently not necessarily associated with a transition to non-marine habitats.



2000 ◽  
Vol 203 (11) ◽  
pp. 1671-1678 ◽  
Author(s):  
C.G. Farmer ◽  
D.R. Carrier

A number of anatomical characters of crocodilians appear to be inconsistent with their lifestyle as sit-and-wait predators. To address this paradoxical association of characters further, we measured lung ventilation and respiratory gas exchange during walking in American alligators (Alligator mississippiensis). During exercise, ventilation consisted of low-frequency, large-volume breaths. The alligators hyperventilated severely during walking with respect to their metabolic demands. Air convection requirements were among the highest and estimates of lung P(CO2) were among the lowest known in air-breathing vertebrates. Air convection requirements dropped immediately with cessation of exercise. These observations indicate that the ventilation of alligators is not limited by their locomotor movements. We suggest that the highly specialized ventilatory system of modern crocodilians represents a legacy from cursorial ancestors rather than an adaptation to a lifestyle as amphibious sit-and-wait predators.



2005 ◽  
Vol 103 (3) ◽  
pp. 567-575 ◽  
Author(s):  
Steven L. Jinks ◽  
Richard J. Atherley ◽  
Carmen L. Dominguez ◽  
Karen A. Sigvardt ◽  
Joseph F. Antognini

Background Although volatile anesthetics such as isoflurane can depress sensory and motor neurons in the spinal cord, movement occurring during anesthesia can be coordinated, involving multiple limbs as well as the head and trunk. However, it is unclear whether volatile anesthetics depress locomotor interneurons comprising central pattern generators or disrupt intersegmental central pattern generator coordination. Methods Lamprey spinal cords were excised during anesthesia and placed in a bath containing artificial cerebrospinal fluid and D-glutamate to induce fictive swimming. The rostral, middle, and caudal regions were bath-separated using acrylic partitions and petroleum jelly, and in each compartment, the authors recorded ventral root activity. The authors selectively delivered isoflurane (0.5, 1, and 1.5%) only to the middle segments of the spinal cord. Spectral analyses were then used to assess isoflurane effects on central pattern generator activity and coordination. Results Isoflurane dose-dependently reduced fictive locomotor activity in all three compartments, with 1.5% isoflurane nearly eliminating activity in the middle compartment and reducing spectral amplitudes in the anesthetic-free rostral and caudal compartments to 23% and 31% of baseline, respectively. Isoflurane decreased burst frequency in the caudal compartment only, to 53% of baseline. Coordination of central pattern generator activity between the rostral and caudal compartments was also dose-dependently decreased, to 42% of control at 1.5% isoflurane. Conclusion Isoflurane disrupts motor output by reducing interneuronal central pattern generator activity in the spinal cord. The effects of isoflurane on motor output outside the site of isoflurane application were presumably independent of effects on sensory or motor neurons.



2000 ◽  
Vol 203 (22) ◽  
pp. 3505-3512 ◽  
Author(s):  
R.J. Wilson ◽  
M.B. Harris ◽  
J.E. Remmers ◽  
S.F. Perry

While little is known of the origin of air-breathing in vertebrates, primitive air breathers can be found among extant lobe-finned (Sarcopterygii) and ray-finned (Actinopterygii) fish. The descendents of Sarcopterygii, the tetrapods, generate lung ventilation using a central pattern generator, the activity of which is modulated by central and peripheral CO(2)/H(+) chemoreception. Air-breathing in Actinopterygii, in contrast, has been considered a ‘reflexive’ behaviour with little evidence for central CO(2)/H(+) respiratory chemoreceptors. Here, we describe experiments using an in vitro brainstem preparation of a primitive air-breathing actinopterygian, the longnose gar Lepisosteus osseus. Our data suggest (i) that gill and air-breathing motor patterns can be produced autonomously by the isolated brainstem, and (ii) that the frequency of the air-breathing motor pattern is increased by hypercarbia. These results are the first evidence consistent with the presence of an air-breathing central pattern generator with central CO(2)/H(+) respiratory chemosensitivity in any primitive actinopterygian fish. We speculate that the origin of the central neuronal controller for air-breathing preceded the divergence of the sarcopterygian and actinopterygian lineages and dates back to a common air-breathing ancestor.



1969 ◽  
Vol 51 (2) ◽  
pp. 407-430 ◽  
Author(s):  
B. R. MCMAHON

1. The anatomy of the head and branchial region of Protopterus has been studied by dissection and section techniques to show the relation between skeletal and muscular elements. X-ray cinematographic, pressure and electromyographic techniques have been used to show how the muscular and skeletal systems interact to produce the respiratory movements. The mechanisms involved in aquatic and aerial respiration in Protopterus have thus been elucidated. 2. The mechanisms of branchial irrigation has been shown to be basically similar to that seen in teleost and elasmobranch fishes, and also similar to that seen in larval amphibia. 3. The aerial cycle is composed of a series of aquatic-type cycles, each of which is modified slightly to serve a specific function in the aerial cycle. Inspiration occurs by a buccal force-pump mechanism. Expiration occurs by the release of compressed pulmonary gas, aided by the elasticity of the lung wall. 4. In this animal the air-breathing mechanism is derived from the aquatic mechanism. The modifications are relatively simple and produce an efficient ventilation mechanism. 5. No movements of the ribs can be seen associated with the respiratory cycles. It is suggested that the aspiratory ventilation mechanisms were not present in the prototetrapods and were not evolved until a later, more fully terrestrial stage was reached. 6. The evidence suggests that the air-breathing mechanism of the tetrapods was powered by a buccal force-pump mechanism which evolved directly from the aquatic system. The evolution of a new mechanism for lung ventilation in the prototetrapods is considered unnecessary.



1987 ◽  
Vol 65 (2) ◽  
pp. 348-353 ◽  
Author(s):  
David J. Bevan ◽  
Donald L. Kramer

Clarias macrocephalus are continuous, facultative air breathers. Individuals (7.6–20.9 g) survived more than 25 days in normoxic water without surface access. Buoyancy decreased and water-breathing frequency increased when surface access was denied, but growth rate and the frequency of air-breathing attempts did not change. We examined air-breathing and water-breathing frequency in shallow (60 cm) and deep (235 cm) water under normoxic (8.0 mg O2∙L−1) and hypoxic (0.3, 0.7, 1.2, and 2.0 mg O2∙L−1) conditions to examine how changes in the travel costs of breathing affected the use of each respiratory mode. Air-breathing and water-breathing frequency increased as dissolved oxygen decreased from 8.0 to 2.0 mg O2∙L−1. Below this level air breathing continued to increase, but water breathing dropped sharply. At higher levels of dissolved oxygen (8.0 and 2.0 mg O2∙L−1), fish in deep water had lower air-breathing and higher water-breathing frequencies than fish in shallow water. Vertical distance travelled and time spent in air breathing increased with increasing depth and with decreasing level of dissolved oxygen. These results support the hypotheses that travel is a significant cost of aerial respiration and that fish respond to increases in this cost by decreasing their use of atmospheric oxygen when dissolved oxygen concentration permits them to do so.



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