determine, if possible, the nature of the nerve-supply to the pulmonary perfused with a saline solution, and the effects were observed of stimulating
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1 : : : OBSERVATIONS ON THE PERFUSED LUNGS OF THE GUINEA- PIG. By ALISON S. DALE 1 and B. NARAYANA. From the Departments of Physiology, University of Birmingham and University of Edinburgh. (Received for publication 6th February 1935.) THE nature of the nerve-supply to the pulmonary vascular system has been the subject of many investigations, but the results obtained by the various investigators are by no means in agreement, no doubt principally on account of differences in the animals and experimental methods which have been employed. Thus, while many workers have found definite evidence of a nervous control of the pulmonary vascular system in the mammal, others have obtained negative results. [For references see the review by Daly, 1933.] The large majority of these experiments have been made on the lungs of the dog, cat or rabbit, while the observations on the nervous control of the pulmonary vessels of the guinea-pig are comparatively few in number, and such as are available show remarkably conflicting results. These observations are nearly all concerned with the action of adrenaline, and the recorded actions of this drug include constriction or dilatation [Tribe, 1912], no effect [Baehr and Pick, 1913] and constriction, no effect or dilatation [Ettinger, 1929, 1931]. It seemed desirable, therefore, to make further experiments with the lungs of the guinea-pig, and to determine, if possible, the nature of the nerve-supply to the pulmonary vessels. All the experiments of the present series were made on lungs perfused with a saline solution, and the effects were observed of stimulating the cervical vagus and thoracic sympathetic nerves, and of injecting acetylcholine and adrenaline. METHODS. The perfused lung preparation was made in the following manner. In the majority of experiments the animal was killed by a blow on the neck, though in some of the earlier experiments it was anoesthetised by nembutal (10 mg. per 100 g. intraperitoneally). A tracheal cannula was inserted, the chest opened and artificial respiration started. 1 Beit Memorial Research Fellow. The earlier part of this work was carried out during the tenure of the George Henry Lewes Studentship.
2 86 Dale and Narayana Cannulae were then tied into the pulmonary artery and the left auricle, and perfusion begun immediately. The perfusion pressure varied, in different experiments, between 4 and 10 cm. of saline, and was maintained from a reservoir of perfusion fluid warmed to a temperature of 400 C. and constantly bubbled with pure oxygen or oxygen and 7 per cent. CO2. From the reservoir the fluid passed through a glass spiral which was immersed in a water-bath maintained at a temperature of 400 C., and thence to the inflow cannula. The rate of outflow of the perfusion fluid was measured by means of a thermionic drop recorder [Harris, 1931], and in the later experiments the respiratory pressure was also recorded by means of the pump described by Daly, Peat and Schild [1935]. In those experiments in which the effect of nerve stimulation was to be observed the nerves were isolated and the stimulating electrodes placed in position before inserting the perfusion cannulae, so that the nerves could be stimulated immediately after beginning the perfusion. This is a very necessary precaution, as once perfusion has started the nerves rapidly lose their excitability. Drugs were injected into the rubber tubing leading to the inflow cannula, the injection syringe and its contents having previously been warmed in the water-bath to avoid any effects on the flow due to changes in temperature of the perfusion fluid. Three kinds of perfusion fluid were used. In the majority of experiments of the first series the fluid was made up according to Locke's original formula (NaCl, 0-92 g.; KC1, g.; CaCl2, g.; NaHCO3, g./100 c.c. distilled water), and this was bubbled with oxygen and 7 per cent. CO2. A few experiments were made using a phosphate buffered Ringer (NaCl, 0-85 g.; KCl, g.; CaCl2, g.; Na2HPO4, 0-06 g./100 c.c. distilled water) bubbled with oxygen. In a later series of experiments a hypertonic Tyrode's solution was used (NaCl, 0-8 g.; KCl, 0-02 g.; CaCl2, 0.01 g.; MgCl2, 0.01 g.; NaH2PO4, g.; NaHCO3, 041 g./80 c.c. distilled water). The experiments were carried out in two series, the first in Birmingham from January to September 1933 (A. S. D.) and the second in Edinburgh from July to December 1934 (B. N.); both authors cooperated occasionally in Edinburgh. EFFECT OF NERVE STIMULATION. 1. The Vagi.-Stimulation of the cervical vagi was carried out in eleven experiments. In the first six of these, which belong to the first series, the animal was ansesthetised with nembutal and the lungs were perfused with bicarbonate buffered fluid. In three of the experiments there was no effect, and in the other three a very slight increase or decrease in flow was observed. The periods of stimulation were always short, never exceeding 30 seconds in duration. In the experiments of
3 Observations on the Perfused Lungs of the Guinea-pig the secohl series the animal was not antesthetise(i but killed by a blow on the neck, and the lungs were perfused with hypertonic Tyrode solution. In three of these, in w-hiclh the respiratory pressure was recorde(1 as wnell as the flow of perfusion fluid, stimulation of the vagi caused a clinminution in the flow accompanied by an increase in respiratory pressure (fig. 1, a). Previous injection of )0 y eserine did not augment the effects of stimulation of the vagi in this latter series. In these exl)eriients the effects only appeared after a considerable latent period (15-30 seconds); this may partly explain the absence of any effect in the first series of experimen-its in which the period of stimulation 87 a b Fic. 1.-Effect of Xvaguls stinitiulatioii on rate of oiitflowx from guinea-pig's lungs: (a) During rhythm-ic inflation, vagi stimulated betw~een arrows. (b) Durinig mi-aintained inflation of lungs; vagi stimulate(1 between arrows. (c) Effect on outflow of raising resp)iratory pressure by increasing stroke of respiration pumip. At first arrow stroke increased, at secon(1 arrow (lecreasedl. In this and in figs. 2, 3, 6 and 7, uipper tracing shows respiratory pressure, middle tracing dirop record of outflowv, lower truein-g timie in minutes. never exceeded 3(0 seconds. In the two remaining experimi-ents of this series, however (to be described below), this latent period was not observed, and cannot therefore be the sole explanation of the negative results of the first series; it is possible that the antesthetic in1ay have beeni a partial cause. In considlering the effects of the vagius stimulation in the second,series we niust take into account the possible effects on the flow of the rise of respiratory pressure. This rise is the result of bronchoconstriction, and when this occurs the lungs cannot collapse, and so remain in a permanently inflated condition. It has been known for many years [de Jager, lss5] and confirmed in the present experimients (see fig. 1, c) that inflation of the lungs by positive pressure reduces the flow through the vascular syst em, and it seemed! possible that the (liminlition of flown observed (luring vagus stimulation might also be tile result of the iniflated state of the lungs. To test this possibility
4 88 Dale and Narayana two further experiments were performed, in which the vagus was stimulated while the lungs were maintained in a permanently inflated condition by blowing them up and clamping the tracheal tube. Vagus stimulation then still produced a diminution in flow, which in all probability was the result of contraction of the vascular musculature (fig. 1, b). In this connection it has been shown that pulmonary vasomotor effects may take place in the absence of any alteration in bronchial calibre [Daly and Euler, 1932]. No definite evidence was obtained of the presence of vasodilator fibres in the vagus, though in one of the last two experiments of the second series a slight increase in flow preceded the "!" a b FIG. 2.-Abolition of vagus effect by atropine. Vagus stimulated between arrows (a) before atropine, (b) 8 minutes after injection of 500 y atropine into arterial cannula. usual decrease in the latter three of a group of six vagus stimulations. Great stress is not laid on this result, however, as the flow was somewhat irregular in the latter part of the experiment, and the increases observed may have been spontaneous ones which chanced to coincide with the beginning of the period of stimulation. The vasomotor and bronchomotor effects of vagus stimulation were both abolished by atropine (fig. 2). 2. The Thoracic Symiipathetic. In another series of experiments the stellate ganglion wleas exposed and stimulated; the animal Aw-as ana-sthetised with nemnbutal, and the bicarlbonate buffered solution perfused. In three experiments the results were negative, but in one positive experiment the stimulation pro(luced a very pronounced decrease in the rate of flow, and control stimulations showed that this effect, was not, due to current spread exciting other structures. Injection of 250 y ergotamine abolished the effect l)ut, did not reverse it. This
5 Observations on the Perfused Lungs of the Guinea-pig 89 one positive result suggests that the stellate ganglion sends vasoconstrictor fibres to the pulmonary vessels of the guinea-pig, but gives no evidence of vasodilator fibres. It should be recalled that Euler [1932] was unable to elicit pulmonary vasomotor effects on excitation of the stellate ganglion during perfusion of rabbits' lungs: he attributed this result to death of the vasomotor fibres. ACTION OF ACETYLCHOLINE. The action of acetylcholine was studied in the first series of experiments, using bicarbonate buffered perfusion fluid and a fast perfusion rate. Doses of 5, 10, and 20 y were tested and the effect on the outflow recorded. The respiratory pressure was not recorded in these experiments, but artificial respiration was applied and the condition of the lungs noted before and after the injections of acetylcholine. The effect of acetylcholine on the outflow was always a diminution, though the intensity of the effect varied in different experiments-from a scarcely perceptible decrease to a very pronounced one. An increase of flow was never observed under these conditions. Curve (1) in fig. 4 shows a typical example of the acetylcholine effect. Inspection of the lungs showed that after an injection of acetylcholine they became rigid, indicating bronchoconstriction; this observation has been confirmed in a later series of experiments in which the respiratory pressure has been recorded. The acetylcholine effect was abolished after injection of 0 1 or 0 5 mg. atropine. No intensification of the effect was observed after injection of 50 y (one experiment) or 650 y of eserine (one experiment), nor during perfusion with a fluid containing 1/1 million eserine (one experiment). In the second series of experiments the effect of acetylcholine was investigated on the flow from the pulmonary vessels and on the respiratory pressure during perfusion with hypertonic Tyrode's solution and using a slower rate of flow. Acetylcholine in doses varying from 0 5 y to 50 y then always caused vasoconstriction and bronchoconstriction (fig. 3, a), except in one experiment in which vasodilatation combined with bronchoconstriction was obtained with 10 y and 20 y acetylcholine. The perfusion pressure in this experiment was 10 cm. Tyrode, while in all other experiments the pressure was maintained between 4 cm. and 8 cm. Previous treatment with 250 y atropine always abolished the vasoconstriction and bronchoconstriction produced by acetylcholine. In only one experiment of this series was intensification of the action of acetylcholine after 50 y eserine observed. In interpreting the results of these experiments the possibility again arises that the decrease in outflow may be secondary to the rise of respiratory pressure which also occurs. Inspection of the tracings obtained has shown, however, that in three instances, in different
6 90 Dale and Narayana experiments, injection of acetylcholine in the usual dosage produced a decrease in outflow which was not accompanied by any significant change of respiratory pressure (fig. 3, b). In all three cases this occurred at the end of the experiment and after several injections of adrenaline. Further, in two experimients in which artificial respiration was not applied but the lungs were maintaine(d in an inflated condition by blowing thein up and clamping the tracheal tube, injection of acetylcholine produced the usual diminution of outflow (fig. 3, c), and in a b c FIG. 3.-Effect of acetyicholine on outflow fromn perfused guinea-pig's lungs: (a) During rhythmic inflation; at arrow 1, acetylcholine injected. (b) For description see text: at arrow 20 y acetylcholine injected. (c) During maintained inflation of lungs; at arrow 5 y acetylcholine injected. some of the experiments of the first series in which the lungs remained deflated throughout the experiment the action of acetylcholine on the outflow weas still the same. ENHANCEMENT OF THE ACETYLCHOLIN-E EFFECT BY ADRENALINE. In some of the experiments of the first series it was noticed that, after an injection of adrenaline, a dose of acetylcholine produced a greater diminution in the outflow than that produced by the same dose before giving the adrenaline, and this apparent action of adrenaline a-as tested further in a series of experiments in which the effects of given doses of acetylcholine were observed during perfusion with fluid containing adrenaline, and compared with those of the same doses injected (luring previous and subsequent perfusion with normal fluid. Several concentrations of adrenaline wnere tried, and it waas found that, while a concentration of 1/1 million produced little alteration in the acetylcholine effect, concentrations of 1/ 250,000 or more produced a pronounced intensification. In some of the experiments a still further
7 Observations on the Perfused Lungs of the Guinea-pig intensification was observed when the adrenaline-containing fluid was replaced by normal fluid, the normal acetylcholine response only returning later. In other experiments this return was incomplete, and it was noted that in these experiments Parke, Davis and Co.'s adrenaline chloride with chloretone had been used. In the remainder of the experiments the Burroughs-Wellcome tabloid preparation was employed. The result of an experiment is shown in fig. 4. The perfusion with (_ (4. 10 (! (3)f1+ Fia Effect of adrenaline upon action of acetylcholine on outflow from left auricle. At arrows injections of 5y acetylcholine into inflow cannula: (1) perfusion with normal bicarbonate Ringer; (2) perfusion with 1/250,000 adrenaline; (3) 2 minutes after replacing adrenaline solution with normal Ringer; (4) 17 minutes after (3). Ordinate drops per 15 see., abscissa time in minutes. adrenaline always decreased the outflow, and in order to make the results comparable the perfusion pressure was adjusted so that the initial flow was approximately the same before each injection of acetylcholine. An attempt was made to investigate this phenomenon further. As stated above, perfusion with adrenaline always decreased the outflow, indicating a probable vasoconstriction, and it seemed possible that this increase in tone of the vessels might play some part in the intensification of the acetylcholine effect. Four experiments were therefore made in which vasoconstriction was produced by perfusion with fluid containing barium chloride and the effect on the action of acetylcholine observed. A concentration of 1/2000 BaCl2 was used, as this was found to produce about the same degree of vasoconstriction as 1/250,000 adrenaline. The effect of this concentration of adrenaline was always tested later in the same experiment. The results obtained with barium chloride were as follows. In two of the experiments an intensification of the acetylcholine effect was produced, which disappeared slowly on replacing the barium chloride solution with normal fluid, in one experiment a slight further intensification being observed. The intensification produced by subsequent perfusion with 1/250,000 adrenaline was in both experiments greater than that produced by the barium chloride (see fig. 5). In a third experiment, however, perfusion with barium chloride reversed the acetylcholine effect. While injection of 10 y acetylcholine produced the usual diminution of flow during perfusion with the normal fluid, during perfusion with 1/2000 barium
8 92 Dale and Narayana chloride the same dose produced an increase in flow. On changing back to normal fluid the effect was again a diminution, and this diminution was intensified by subsequent perfusion with 1/250,000 adrenaline. These effects are shown in the lower part of fig. 5. In the fourth experiment the effect of acetylcholine was unchanged by perfusion with barium chloride. In discussing the significance of these effects three possible explanations must be taken into account, namely: (1) that the enhancement is the result of changes in the tone of the bronchial musculature produced by adrenaline; (2) that it is the result of changes in the tone of the pulmonary blood-vessels produced by adrenaline; (3) that 125t' 20 ; $X /5 _ (1) (X) (3) (i) (2.) (3) (4) 15 _,,,,,.,, FIG. 5.-Effects of barium chloride and of adrenaline upon action of acetylcholine on outflow from left auricle. Above, At arrows injection of 5 y acetylcholine into inflow cannula: (1) perfusion with normal bicarbonate Ringer; (2) perfusion with 1/2000 BaCl2; (3) 22 minutes after replacing BaCl2 solution with normal Ringer; (4) perfusion with 1/250,000 adrenaline. Below, At arrows injection of 10 y acetylcholine: (1) perfusion with normal bicarbonate Ringer; (2) perfusion with 1/2000 BaCl2; (3) 22 minutes after replacing BaCl2 solution with normal Ringer; (4) perfusion with 1/250,000 adrenaline. Ordinate drops per 15 sec., abscissa time in minutes. it is due to a direct sensitisation of the muscle of the pulmonary bloodvessels to acetylcholine by adrenaline. The first possibility is unlikely in view of the fact that during all the experiments of this series the lungs remained deflated, and effects such as those described earlier in this paper in connection with the effects of vagus stimulation and acetylcholine could therefore not come into play. The second explanation seems more reasonable, in view of the fact that, in two experiments, perfusion with 1/2000 barium chloride, which increased the tone 'of the blood-vessels to about. the same extent as perfusion with 1/250,000 adrenaline, enhanced the effect of acetylcholine, though, on the other hand, it must be remembered that in another experiment perfusion with barium chloride reversed the effect of acetylcholine, while in a fourth it produced no change. Some more recent experiments, however, made in the second series and using slower rates of flow, support such an explanation. It was found in these experiments that with the slower flows the initial effect of acetylcholine was greater than
9 Observations on the Perfused Lungs of the Guinea-pig that observed in the experiments with the fast flows, and that this effect was not enhanced by subsequent perfusion with 1/250,000 adrenaline. This suggested that the conditions of tone obtaining in the blood-vessels with the slower flows were optimal for the action of acetylcholine, and it seemed possible that in the experiments with fast rates of flow the action of adrenaline, and in some cases barium chloride, might be to bring the condition of the blood-vessels nearer the optimal. What this condition may be is not clear; it is evidently not the rate of flow itself, for in the experiments in which the enhancement by adrenaline was observed care was taken to maintain the rate of flow constant throughout the experiment. It may be noted in this connection that Berry and Daly [1932], working on the isolated perfused lungs of the dog, observed in one experiment that acetylcholine caused vasoconstriction at low and vasodilatation at high perfusion pressures, an effect which could be obtained repeatedly. That the enhancement of the acetylcholine effect produced by adrenaline may be the result of a direct sensitisation of the blood-vessels is supported by the similarity of this effect to an enhancement observed by Dale and Gaddum [1930] in denervated voluntary muscle. Using isolated strips of the denervated diaphragm of the cat they found that addition of adrenaline to the fluid in the bath in which the strip was immersed caused a pronounced enhancement of the contracture produced by acetylcholine, and, further, that this enhancement increased immediately after replacing the adrenaline-containing fluid with fresh Ringer's solution, the contraction only later returning to normal. A similar enhancement of the acetylcholine effect by adrenaline followed by a still further enhancement when the adrenaline-containing solution was replaced by fresh Ringer's solution was observed in the present experiments (see fig. 4), and it is tempting on these grounds to conclude that here also the action of adrenaline is to sensitise the vessel to acetylcholine. It must be remembered, however, that the enhancement is only observed when the rate of flow of perfusion fluid through the pulmonary vessels is relatively fast, no enhancement being observed with slow rates of flow; and further, that in one of the two experiments in which barium chloride enhanced the effect of acetylcholine a slight further enhancement was observed during the period in which the barium chloride was being washed out by fresh Ringer's solution. The true explanation of this effect can evidently only be determined by further experiment. The results so far obtained make one point clear, namely, that the effect on the pulmonary blood-vessels of a drug such as acetylcholine is greatly affected by changes in perfusion pressure or by previous treatment with other drugs, and it seems possible that the variation in the results obtained by previous workers may be explained by differences in the conditions of experimentation 93
10 94 Dale and Narayana determining the initial tension, length and tone of the smooth muscle fibres of the blood-vessels. One of the results described above throws further light on the action of acetylcholine. The fact that in one experiment, during perfusion with 1/2000 barium chloride, injections of acetylcholine consistently produced an increase in the outflow, shows that under suitable conditions acetylcholine can produce vasodilatation in the lungs of the guinea-pig. EFFECT OF ESERINE. While investigating the effect of eserine on acetylcholine it was noticed that eserine in itself caused a diminution in outflow with bronchoconstriction in doses of 50y in six experiments and 500 y in two experiments. The diminution in outflow was observed soon after the injection of eserine, but the bronchoconstriction only appeared later, in some of the experiments after a latent period of even 10 minutes. These vascular and bronchial effects of eserine were seen whether injections of acetylcholine had previously been given or not. Atropine in doses of 50 y and 250 y injected previously did not prevent the effects of eserine either on the vessels or on the bronchi. In two experiments an injection of 50y eserine following 250 y atropine caused a slight increase in flow before the decrease set in. ACTION OF ADRENALINE. As has already been mentioned, previous workers have obtained conflicting results with regard to the action of adrenaline on the pulmonary blood-vessels of the guinea-pig. While Baehr and Pick [1913] observed no effect on lungs perfused with Tyrode solution, Tribe [1912] obtained constriction with pure adrenaline, and dilatation with adrenaline which contained chloretone as a preservative. Ettinger [1929] observed constriction, but only at certain seasons of the year; he found no effect, or a slight dilatation, at other times. The present experiments were carried out in two series. The first from January to September (excluding August) 1933, and the second from July to November In the first series adrenaline in doses of 5, 10 or 20 y always produced the same effect, namely, a decrease in the rate of outflow of the perfusion fluid though the intensity of the effect varied in different experiments. No indication was found of the seasonal variation described by Ettinger, and no difference was observed between the actions of pure adrenaline and adrenaline with 0 5 per cent. chloretone, such as was found by Tribe. In this series, though the respiratory pressure was not recorded, the condition of the lungs was noted, and it was found that when the lungs were rigid as a result of
11 Observations onl the Perfused Lungs of the (4tinea-p 95, bronichoconstriction injection of adrenaline alw avs restored themn to normal. In the secon(1 series of experiments in wh-hich the lhypertonic TyroIels solution was perfused and the respiratory pressure recorded simuiiltaneously with the rate of outflow, the follown-ing observations wa-ere made. It was noticed that the effect of adrenaline on the outflow depended to some extent on the state of the tone of the bronchial tubes at the time of injection. If the respiratory pressure wn-as low, indicating bronchodilatation, injection of adlrenaline (1-So0 y) always produced a decrease ill the outflow, which was not accompanied by any significant change in the respiratory pressnre (see fig. 6, a and c). On the other (.L () C Fic'l. 6.- Effeet of adren-1alinel 011 Outflow froi1 p)(i'fuel guinea-pjig's lingsrs at difterent initial respiratory pressiures. 2)0 1a(renaliIie Injeete(dI at arrows: ((a) at low pressure; (b) after thle respiratorn pressure hlad been raie(l s ) injeetioi of acetlh lelolie; (c) a few minutes -after (b). hand, if the respiratory pressure u-as high, indicating bronchoconstriction, injection of adrenaline over the same range of (loses always produced a fall of the respiratory pressure due to bronchodilatation, w-hich w-as occasionally accoimpanied by increase inl the outflow (see fig. 6, 1) and sometimues b)y very slight constriction. It seems possible that the increase in outflow observedl undler the latter conditions might have a merely mechanical cause, namely, the diminution in intrapulmonary pressure which resulted from the bronclhodilatation, since we had found (fig. 1, c) that inflation of the lungs (lecreased the rate of flow through the puilmonary -vessels, the flow increasing again wlhen the lungs collapsed. To test this possibility some experiments w ere perforiued in w bilich injections of adrenaline wa-ere made while the lungs were maintainel in an1 inflated condition, so that a fall in the tone of
12 96 Dale and Narayana the bronchial tubes could not cause a diminution in the intrapulmonary pressure. Adrenaline then always produced a diminution of the outflow, suggesting that the increased flow described above had a purely mechanical cause (fig. 7). FiG Effect of adrenaline on outflow from perfused guinea-pig's lungs during maintained inflation of lungs. At arrow 10 y adrenaline injected. SUMMARY. In the isolated guinea-pig's lungs, perfused through the pulmonary artery with modified Ringer or Tyrode solution: 1. Excitation of the cervical vagi, or injection of acetylcholine, causes bronchoconstriction and vasoconstriction. These effects are abolished by atropine but are unaffected by eserine. Acetylcholine caused vasodilatation in one experiment only. 2. In one out of four experiments excitation of the stellate ganglion caused vasoconstriction. Injection of adrenaline produces vasoconstriction and, if the tone of the bronchial muscles is already high, bronchodilatation. 3. During rhythmic inflation bronchoconstriction diminishes flow and bronchodilatation increases it. During the action of a drug affecting both bronchi and blood-vessels tw o mechanisms are responsible for the final effect upon the blood-vessels: (a) the action of the drug upon the blood-vessels and their peripheral elements, and (b) the mechanical forces exerted on the blood-vessels as a result of concomlitant changes in bronchial calibre. The resultant effect is the algebraic sunm of the two effects. 4. Eserine causes bronchoconstriction and vasoconstriction in atropinised preparations. We wish to express our thanks to Professor I. de Burgh Daly for suggesting this work and for his advice and encouragement throughout. The expenses of this research were in part defrayed by a grant to one of us (B. N.) from the Moray Endowment Committee, to whom we express our thanks.
13 Observations on the Perfused Lungs of the Guinea-pig 97 REFERENCES. BAEHR, V. G., and PICK, E. P. (1913). Arch. exp. Path. Pharm. 74, 65. BERRY, J. L., and DALY, I. DE BURGH (1932). Quoted by Daly (1933), infra. DALE, H. H., and GADDUM, J. H. (1930). J. Physiol. 70, 109. DALY, I. DE BURGH (1933). Physiol. Rev. 13, 149. DALY, I. DE BURGH, and VON EULER, U. S. (1932). Proc. Roy. Soc. B, 110, 92. DALY, I. DE BURGH, PEAT, S., and SCHILD, H. (1935). 25, 33. DE JAGER (1885). Pflugers Arch. 36, 309. ETTINGER, G. H. (1929). J. Physiol. 67, 42 P. ETTINGER, G. H. (1931). Quart. J. Exp. Physiol. 21, 59. EULER, U. S. VON (1932). J. Physiol. 74, 271. HARRIS, D. T. (1931). J. Physiol. 71, 22 P. TRIBE, E. M. (1912). J. Physiol. 45, 21 P. Quart. J. Exp. Physiol. VoI,. XXV., No 1.-19:35. 7,
blood-vessels of the isolated perfused lungs of the rat. Both Hirakawa
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