Breathing movements in the frog Rana pipiens. I. The mechanical events associated with lung and buccal ventilation

1975 ◽  
Vol 53 (3) ◽  
pp. 332-344 ◽  
Author(s):  
N. H. West ◽  
D. R. Jones

The normal pattern of breathing movements in Rana pipiens has been studied by recording pressure and volume changes in the buccal cavity and lungs, and electromyograms from the muscles involved in this activity. Two types of breathing movement were obtained, one concerned with ventilation of the buccal cavity (buccal cycles) and the other with lung ventilation (lung cycles). Only in the latter type of movement were the nares and glottis actively involved. During buccal cycles the nares remained open and the glottis closed, so although excursions of the buccal floor were some two-thirds of the magnitude of those occurring during lung cycles, only low pressures were generated. The onset of a lung cycle was signalled by activity in the laryngeal dilator muscle. When the glottis opened, lung pressure and volume decreased, and buccal cavity pressure and volume increased. After closure of the nares, the buccal floor was rapidly elevated by the activity of the breathing muscles and air was forced into the lungs from the buccal cavity. At peak pressure in the lungs and buccal cavity the glottis closed and nares opened. The recovery stroke of the buccal pump was passive. No evidence was found for large pressure differentials between the buccal cavity and lungs when the glottis was open, and air-flow recordings at the external nares showed two phases of flow during each buccal cycle and four phases with each lung ventilation cycle.

1976 ◽  
Vol 64 (1) ◽  
pp. 25-38
Author(s):  
N. H. West ◽  
D. R. Jones

1. Diving apnoea in Rana pipiens was initiated by submerging the external nares. As the water level was raised above the frog, both buccal and lung pressure increased by an amount corresponding to the water head. During submergence the external nares remained closed, although the apnoeic period was punctuated by ventilation movements which moved gas between the lungs and buccal cavity. 2. Bilateral section of the ophthalmic nerves did not alter the normal pattern of ventilation in air, although it often resulted in the intake of water into the buccal cavity on submergence. Introduction of water into the buccal cavity, either naturally as in denervates or by injection through a catheter in intact frogs, triggered sustained electromyographical activity in some respiratory muscles. 3. Electroneurograms recorded from the cut peripheral end of an ophthalmic nerve showed that receptors in the external narial region were stimulated by movement of a water meniscus across them. Activity could also be recorded in the ophthalmic nerve in response to water flow past the submerged nares. Punctate stimulation of the narial region confirmed that these receptors were mechanosensitive. 4. Bilateral electrical stimulation of the central ends of cut ophthalmic nerves in lightly anaesthetized frogs caused apnoea with a latency of less than 200 ms. The external nares remained closed throughout the period of stimulation although buccal pressure events, resembling underwater ventilation movements, occurred when stimulation was prolonged.


1998 ◽  
Vol 201 (5) ◽  
pp. 673-682 ◽  
Author(s):  
E L Brainerd ◽  
J A Monroy

Lung ventilation in Siren lacertina was studied using X-ray video, measurements of body cavity pressure and electromyography of hypaxial muscles. S. lacertina utilizes a two-stroke buccal pump in which mixing of expired and inspired gas is minimized by partial expansion of the buccal cavity during exhalation and then full expansion after exhalation is complete. Mixing is further reduced by the use of one or two accessory inspirations after the first, mixed-gas cycle. Exhalation occurs in two phases: a passive phase in which hydrostatic pressure and possibly lung elasticity force air out of the lungs, and an active phase in which contraction of the transverse abdominis (TA) muscle increases body cavity pressure and forces most of the remaining air out. In electromyograms of the lateral hypaxial musculature, the TA became active 200-400 ms before the rise in body cavity pressure, and activity ceased at peak pressure. The TA was not active during inspiration, and no consistent activity during breathing was noted in the external oblique, internal oblique and rectus abdominis muscles. The finding that the TA is the primary expiratory muscle in S. lacertina agrees with findings in a previous study of another salamander, Necturus maculosus. Together, these results indicate that the use of the TA for exhalation is a primitive character for salamanders and support the hypothesis that the breathing mechanism of salamanders represents an intermediate step in evolution between a buccal pump, in which only head muscles are used for ventilation, and an aspiration pump, in which axial muscles are used for both exhalation and inhalation. <P>


1990 ◽  
Vol 154 (1) ◽  
pp. 537-556 ◽  
Author(s):  
TIMOTHY ZOLTAN VITALIS ◽  
GRAHAM SHELTON

The mechanism and pattern of ventilation in unrestrained Rana pipiens were investigated by simultaneous measurements of pulmonary pressure, buccal pressure and air flow at the nostrils. The buccal cavity was ventilated continuously at a rate of 90±3.2oscillations min−1 by low-amplitude pressure swings above and below atmospheric. The lungs were ventilated intermittently by the buccal pump at a rate of 6.3±0.8breathsmin−1. Expiration of gas from the nostrils occurred on two occasions during a lung ventilation. Ventilation of the lungs was achieved by precise timing of two valves, the nostrils and glottis. The timing of the valves determined the volume of expiratory flow on these two occasions and its relationship to inspiratory flow. Thus, the breathing movements could cause inflation, deflation, or no change in the lung volume. Periodically the lung was inflated by a sequence of successive breaths. During inflations the nostrils closed simultaneously with glottal opening and almost no gas was expired during the first expiratory phase. This caused a complete mixing of buccal contents and pulmonary gas and this mixture was pumped back into the lung. Deflations were characterized by a delay in nostril closing that resulted in a large outflow of gas from the lung and buccal cavity during the first phase of expiration. More gas left the system than was pumped into the lungs. The results suggest that coherent air flow from glottis to nostrils, as required by the ‘jet stream’ hypothesis of Gans et al. (1969), is not likely to occur.


1975 ◽  
Vol 53 (3) ◽  
pp. 345-353 ◽  
Author(s):  
N. H. West ◽  
D. R. Jones

The work done by the buccal cavity during buccal and lung ventilation cycles has been estimated from measurement of the area enclosed by pressure–volume loops for each cycle. The loops cycled in an anticlockwise direction with respect to time during buccal cycles. On the other hand, pressure–volume loops from the lungs cycled clockwise, showing that work was being done on the lungs by the buccal pump. Inflation and deflation of the buccal cavity from a syringe, in curarized frogs, gave a clockwise loop enclosing about 5.5–6.5% of the area enclosed by a naturally generated loop of the same pressure and volume. However, inflation and deflation of the lungs gave a loop which enclosed an area virtually identical with that obtained from a normally generated sequence of lung inflation and deflation. The power output of the buccal pump was directly proportional to body weight, the major determinant of the former being the larger buccal volume rather than pressure change as body weight increased. The mechanical efficiency of the buccal pump varied from 0.4% to 16.2%, efficiency increasing with increased power output over most of the physiological range. Mean efficiency of all buccal movements was calculated to be 8% and, at this value of efficiency, oxygen consumption of the respiratory muscles was 0.89 ml O2 100 g−1 min−1. In Rana pipiens at rest the oxygen cost of breathing appears to be about 5% of the total resting metabolism.


1979 ◽  
Vol 80 (1) ◽  
pp. 251-269 ◽  
Author(s):  
S. S. BRETT ◽  
G. SHELTON

1. Lung pressures, buccal pressures, lung volumes, and EMGs from respiratory muscles were measured in unrestrained Xenopus laevis to analyse their roles in the lung ventilation cycle. 2. Lung pressure was always maintained above atmospheric levels and a buccal pumping mechanism was used to fill the lungs in Xenopus, as in other Amphibia. 3. Xenopus, unlike other amphibians, does not ventilate the buccal cavity between lung ventilations. 4. Expiration of gases from the buccal cavity is aided by muscles which decrease buccal cavity volume. Other anurans increase buccal cavity volume during expiration. 5. The buccal phase of inspiration occurs after expired air has passed from the lung and buccal cavity, in comparison to the ranids and bufonids which inspire fresh air into the buccal cavity before expiration.


2000 ◽  
Vol 203 (6) ◽  
pp. 1081-1092 ◽  
Author(s):  
R.S. Simons ◽  
W.O. Bennett ◽  
E.L. Brainerd

The mechanics of lung ventilation in frogs and aquatic salamanders has been well characterized, whereas lung ventilation in terrestrial-phase (post-metamorphic) salamanders has received little attention. We used electromyography (EMG), X-ray videography, standard videography and buccal and body cavity pressure measurements to characterize the ventilation mechanics of adult (post-metamorphic) tiger salamanders (Ambystoma tigrinum). Three results emerged: (i) under terrestrial conditions or when floating at the surface of the water, adult A. tigrinum breathed through their nares using a two-stroke buccal pump; (ii) in addition to this narial two-stroke pump, adult tiger salamanders also gulped air in through their mouths using a modified two-stroke buccal pump when in an aquatic environment; and (iii) exhalation in adult tiger salamanders is active during aquatic gulping breaths, whereas exhalation appears to be passive during terrestrial breathing at rest. Active exhalation in aquatic breaths is indicated by an increase in body cavity pressure during exhalation and associated EMG activity in the lateral hypaxial musculature, particularly the M. transversus abdominis. In terrestrial breathing, no EMG activity in the lateral hypaxial muscles is generally present, and body cavity pressure decreases during exhalation. In aquatic breaths, tidal volume is larger than in terrestrial breaths, and breathing frequency is much lower (approximately 1 breath 10 min(−)(1)versus 4–6 breaths min(−)(1)). The use of hypaxial muscles to power active exhalation in the aquatic environment may result from the need for more complete exhalation and larger tidal volumes when breathing infrequently. This hypothesis is supported by previous findings that terrestrial frogs ventilate their lungs with small tidal volumes and exhale passively, whereas aquatic frogs and salamanders use large tidal volumes and and exhale actively.


1986 ◽  
Vol 251 (5) ◽  
pp. R941-R946
Author(s):  
G. M. Malvin ◽  
M. P. Hlastala

The effects of lung O2 and CO2 content and volume on cutaneous gas exchange and perfusion were investigated in the frog, Rana pipiens. (Ha)-anesthetized frogs were equilibrated with 9.5% Freon-22 (Fr, chlorodifluoromethane) and 1.1% Ha. Cutaneous elimination of Fr, Ha, and CO2 into a small sample chamber on the abdomen was measured with a mass spectrometer. Introducing an air mixture into the lung decreased cutaneous Fr, Ha, and CO2 elimination. Lung inflation with an O2 mixture decreased cutaneous gas elimination more than with the air mixture. Inflation with a N2 mixture had no effect. The response to lung inflation with the air mixture was not affected by adding 4.8% CO2 to the air mixture or by atropine. Voluntary lung ventilation decreased CO2 and Fr elimination. The results indicate that intrapulmonary O2 is a factor regulating skin breathing. If a change in lung volume is also a factor, it requires a concomitant change in lung O2. Intrapulmonary CO2 and cholinergic nerves are not involved in cutaneous respiration across the abdomen.


1998 ◽  
Vol 201 (20) ◽  
pp. 2891-2901 ◽  
Author(s):  
EL Brainerd

The larval stage of the tiger salamander Ambystoma tigrinum is entirely aquatic, but the larvae rely on their lungs for a large proportion of their oxygen uptake. X-ray video and pressure measurements from the buccal and body cavities demonstrate that the larvae inspire using a two-stroke buccal pump and exhale actively by contracting the hypaxial musculature to increase body pressure. Larvae begin a breath by expanding the buccal cavity to draw in air through the mouth, while simultaneously exhaling air from the lungs to mix with the fresh air in the buccal cavity. The mouth then closes, and the buccal cavity compresses to pump a portion of the mixture into the lungs. The remaining air in the buccal cavity is then released as bubbles from the mouth and gill slits. Ventilatory volumes estimated from X-ray video records indicate that approximately 80 % of the air pumped into the lungs is fresh air and 20 % is previously expired air. Exhalation in larval tiger salamanders is active, powered by contraction of all four layers of lateral hypaxial musculature. Electromyography indicates that the transverse abdominis (TA) muscle is active for the longest duration and shows the highest-amplitude activity, but the external oblique superficialis, the external oblique profundus and the internal oblique also show consistent, low-level activity. The finding that the TA muscle is active during exhalation in larval tiger salamanders contributes to a growing body of evidence that the use of the TA for exhalation is a primitive character for tetrapods.


1986 ◽  
Vol 126 (1) ◽  
pp. 453-468 ◽  
Author(s):  
A. W. Pinder ◽  
W. W. Burggren

Pulmonary and cutaneous oxygen uptake (MO2) and lung ventilation were measured in frogs floating in water with access to air in respirometers, with and without ventilation of the skin provided by stirring. The frogs were exposed to hypoxia in both water and air, and were variably active. In inactive frogs floating in unstirred respirometers at 25 degrees C, 23% of total MO2 is through the skin. Activity of the animal increases total MO2. and also ventilates the skin, so that cutaneous MO2 increases with increasing total MO2. When the respirometer is stirred, cutaneous MO2 increases to 35% of total MO2 in resting animals. Activity no longer affects cutaneous MO2. Lung ventilation volume is directly proportional to lung ventilation rate in normoxia. Ventilation rate, and therefore ventilation volume, is proportional to pulmonary MO2. Ventilation rate approximately doubles in hypoxia (PO2 = 52 mmHg). The pattern of ventilation also changes in hypoxia, from a very irregular pattern in normoxia to one showing regular, large oscillations of lung volume over several ventilation movements. Increased lung ventilation, enhancing pulmonary MO2, is the primary adjustment to increased O2 demand. Partitioning of MO2 shifts towards the lung during both activity and hypoxia. In both cases, however, ventilation of the skin can supplement total MO2 by increasing absolute levels of cutaneous MO2.


1994 ◽  
Vol 194 (1) ◽  
pp. 153-165 ◽  
Author(s):  
Q Bone ◽  
E Brown ◽  
G Travers

The respiratory flow of water over the gills of the cuttlefish Sepia officinalis at rest is produced by the alternate activity of the radial muscles of the mantle and the musculature of the collar flaps; mantle circular muscle fibres are not involved. Inspiration takes place as the radial fibres contract, thinning the mantle and expanding the mantle cavity. The rise in mantle cavity pressure (up to 0.15 kPa), expelling water via the siphon during expiration, is brought about by inward movement of the collar flaps and (probably) mainly by elastic recoil of the mantle connective tissue network 'wound up' by radial fibre contraction during inspiration. Sepia also shows a second respiratory pattern, in which mantle cavity pressures during expiration are greater (up to 0.25 kPa). Here, the mantle circular fibres are involved, as they are during the large pressure transients (up to 10 kPa) seen during escape jetting. Active contraction of the muscles of the collar flaps is seen in all three patterns of expulsion of water from the mantle cavity, electrical activity increasing with increasing mantle cavity pressures. Respiratory expiration in the resting squid Loligo vulgaris is probably driven as in Sepia, whereas in the resting octopus Eledone cirrhosa, the mantle circular musculature is active during expiration. The significance of these observations is discussed.


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