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Ventilation and diving apnoea in Rana pipiens West, Nigel Hugh

Abstract

Two types of ventilation cycle were recorded in unanaesthetised but restrained frogs (Rana pipiens); one concerned with ventilation of the buccal cavity alone (buccal cycle) and the other with lung ventilation (lung cycle). During the former the nares were open and the glottis closed so that only small pressures were generated by the movement of the buccal floor. The onset of a lung ventilation was signalled by activity in the laryngeal dilator muscle and when the glottis opened lung pressure and volume fell while buccal cavity pressure and volume increased. After narial closure the buccal floor was rapidly raised and gas 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 pump being passive. Air flow recordings made at the external nares showed two phases of flow during each buccal cycle, while four phases accompanied each lung ventilation cycle. By plotting pressure/volume loops from the buccal pump an analysis was made of the mechanical work performed in one lung ventilation cycle, and the proportion of this work available for lung inflation after various losses against viscous and flow resistive forces in the pump itself; while measurement of the areas of typical sequences of such loops together with respiratory frequency enabled the mechanical work output of the pump to be determined for frogs ranging in size from 24 to 86 grams. Using Hill's classical equation for muscle efficiency, it was possible to estimate mechanical efficiency for single respiratory cycles by calculating the heat of maintenance and heat of shortening of the buccal floor muscles, while simultaneously measuring mechanical work output. Calculated efficiencies of lung ventilation cycles rose as mechanical work performed increased from 7.4% at 0.65 gram.cm/cycle to 19.3% at 2.73 gram.cm/cycle. Diving apnoea in Rana pipiens was induced by the presence of water at the level of the external nares, at which point the nares closed, no water entering the buccal cavity during the dive. Occasional ventilation cycles occurred during the dive in which gas entered the buccal cavity from the lungs, an equal volume then being pumped back into the lungs, but there was no ventilatory exchange with the external medium. Bilateral section of the trigeminal nerves resulted in an abnormal response to submergence, in that water entered the buccal cavity, and in some cases the lungs, while surfacing often did not result in resumption of ventilation. Skin mechanoreceptors in the region of the external narial openings serving the ophthalmic branch of the trigeminal were found to be capable of responding to the minimum stimulus encountered on submersion, movement of a water meniscus across the narial region, while a tonic response to hydrostatic pressure occurred in some preparations. In control experiments cutaneous mechanoreceptors innervated by the spinal nerves were shown to have no response to a water meniscus passing across their receptive fields, suggesting that they possess higher thresholds than the narial receptors. Periods of apnoea could be induced in air in Rana pipiens by bilateral or unilateral stimulation of the cut peripheral ends of the ophthalmic branch of the trigeminal nerve at threshold voltages as low as 30 mv, at a frequency of 200 Hz. Increase in stimulating voltage resulted in longer periods of apnoea before ventilation "broke through", and in these periods the external nares were closed and buccal pressure was held independent of atmospheric pressure. Reduction of the stimulation frequency by a factor of ten after the initiation of apnoea, simulating adaptation of the sensory nerves, proved as effective in maintaining apnoea as continued stimulation at the original frequency.

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