found that stretching increased the oxygen usage within limits but
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1 v qa,.x.- U I di i INFLUENCE OF RESTING LENGTH ON THE OXYGEN USE OF PLAIN MUSCLE. By J. CHRISTODoss DAVID. From the Department of Pharmacology, Edinburgh University. (Received for publication 4th May 1931.) THE oxygen consumption following contraction in both skeletal and cardiac muscle is well known to depend on the resting length of the muscle fibres. Much less is known regarding the influence of length either on the resting metabolism of any form of muscle or on the oxygen consumption of plain muscle, whether contracting or resting. As regards plain muscle, EVANS (1) stated that there is distinctly less oxygen used by uteri of the rabbit and guinea-pig during the tonic state than during the state of relaxation. He concluded that there can be no definite increase of metabolism during the upkeep of tonus. PARNAS (2), experimenting with the adductor muscle of a bi-valve, found that stretching increased the oxygen usage within limits but that extreme extension again reduced the consumption. As regards the resting metabolism of heart muscle, CLARK and WHITE (3) reported that the oxygen use of the filled but arrested auricle of the frog was about double that of the empty and arrested organ. The chief difficulty in estimating the oxygen consumption of muscles is that the tissue is frequently too thick to permit of an adequate diffusion of oxygen through its whole depth even when relaxed; and this condition is aggravated when the muscle is in a contracted state. WARBURG (4) has provided a formula for calculating the supply of oxygen that can diffuse through a given thickness of tissue, viz. d= 8.C.D/A, where d is the thickness in cm. of a section exposed on both sides that will receive an adequate oxygen supply by diffusion, A the observed oxygen consumption of the tissue in c.c. per gram per minute, C the concentration of oxygen in atmospheres, and D Krogh's diffusion coefficient for oxygen, which is 1-4 X 10- at 13 C. Applying this formula I have shown (DAVID (5)) that the rabbit's uterus is too thick to allow adequate diffusion of oxygen; for even when suspended in oxygen it can receive sufficient oxygenation only through about seven-tenths of its thickness. The mouse's uterus is on the border-line, for while the thickness of the immature and dicestrous uterus is just within the " critical " diameter calculated according to HILL'S (6) formula for the diffusion of gases into a cylindrical solid, that of the uterus during cestrus is definitely greater than the "critical " diameter. These facts
2 182 David make the validity of EVANS'S conclusions on the oxygen consumption of the uterus doubtful. METHOD. The frog's bladder is a suitable material for determining the influence of length of muscle fibre on the resting metabolism. Its wall is sufficiently thin to allow proper diffusion of oxygen, and the muscle fibres can be stretched or contracted by varying the filling. I suspended the bladder at the end of a suitable cannula in a Barcroft apparatus filled with oxygen. The apparatus was the same as that used by CLARK and WHITE ((3) fig. la), and each one was calibrated at different fillings. All experiments were conducted at 150 C. in a water-bath fitted with an efficient thermostat. Readings were taken for periods ranging from 4 to 24 hours. Two or more experiments were done with the same bladder, first empty and then filled with 1 or 2 c.c. of oxygenated (frog) Ringer's solution at 150 C., or vice versa. The chief experimental difficulty was that some bladders began to leak after a few hours' isolation. All figures for oxygen consumption were reduced to volumes of dry gas at N.T.P., used per gram of moist tissue per hour or per minute. The frog's bladder is composed of an inner layer of epithelium, and outside this plain muscle fibres mixed with connective tissue. Examination of sections shows that the plain muscle constitutes about 70 per cent. of the whole tissue. I have been unable to measure the proportion of the oxygen consumption due to the plain muscle; it is unlikely that the oxygen consumption of the connective tissue and epithelium would constitute more than 30 per cent. of the total oxygen consumption. EXPERIMENTAL RESULTS. My results are shown in Tables I. and II. In each experiment shown in Table I. the oxygen consumption at two different volumes was measured. Table II. shows the general averages of all experiments. The tables agree in showing that the average oxygen consumption of the filled bladder is about 10 per cent. greater than that of the empty bladder. This difference is so small that it has little significance. DIFFERENCE IN THE SURFACE AREA OF THE EMPTY AND FILLED BLADDER. The surface area of the empty bladder was measured by cutting it open and spreading it out flat on squared paper. It varied from 1l6 sq. cm. to 4 sq. cm. In six bladders, with an average weight of gram, the average area when unstretched was 3-6 sq. cm. I calculated the surface of the bladder filled with known volumes by assuming that
3 Influence of Resting Length on the Oxygen Use of Plain Muscle 183 A. TABLE I. B. Oxygen u se in c.c. Empty. Filling 1-0 c.c. Oxygen use in c.c. Empty. Filling 2-0 c.c TABLE II. A. Oxygen use in c.c. OXYgen USe in C.C. Filling 1 or 2 c.c. B. OxgnueIncc OXYgen USe in C.C. All empty it was quite spherical and using the formula: Surface 4-84 X (Volume)l. According to this, the surface area for 1-0 c.c. filling was 4-84 sq. cm. and for 2-0 c.c., 7-67 sq. cm. My results show, therefore, that even when the surface area of the bladder is more than doubled, there is no certain increase in oxygen consumption. VOL. XXI., NO
4 184 David "CRITICAL" THICKNESS OF THE BLADDER. I calculated the following values for the actual thickness of the bladder and the "critical" thickness for oxygen diffusion according to WARBURG 'S formula: TABLE III. Average weight of Filling in c.c. Observed thickness in cm. " Critical " thick- Ad ness (y in cm. 0*053 0O051 0* * *010 0'007 0*074 0* The maximum thickness of the tissue which, according to WAR- BURG'S formula, would receive an adequate oxygen supply when suspended in oxygen is about five to ten times the actual thickness observed. Therefore the oxygen use of the frog's bladder is not limited by inadequate diffusion of oxygen to any part of the tissue. EVANS (2) found that the oxygen use of the cat's gut varied from 0-28 c.c. per gram per hour for the lower ileum to 0 45 c.c. for the duodenum. Obviously his results were limited by inadequate diffusion of oxygen due to the thickness of the tissue. This is also the most probable explanation for the marked difference reported by him in the oxygen use of the mammalian uteri caused by stretching of the muscle. OXYGEN USE OF DIFFERENT TISSUES OF THE FROG. Table IV. gives the average values obtained by different observers for the oxygen consumption of frog's tissues at rest at 150 C. TABLE IV. Kind of tissue. Whole frog at rest Isolated skeletal muscle of frog Frog's auricle ventricle Frog's bladder Frog's gut. stomach Oxygen use in c.c. per gram per hour at 15 C. 0*05 0* b *3 =\ 0* f Author. MEYERHOF and MEIER (7). MEYERHOF (8). CLARK and WHITE (3). DAVID. FENN (9).
5 Influence of Resting Length on the Oxygen Use of Plain Muscle 185 These figures show that the resting metabolism of plain muscle is nearly twenty times greater than that of striated muscle and between one-half and one-quarter that of cardiac muscle. I measured the weight of the chief tissues of the frog, and these are shown in Table V. as percentages of the total body weight. TABLE V. Kind of tissue. Percentage of total body weight. Skeletal muscle Heart Plain muscle (lungs, stomach, gut, and bladder) Glands (liver, kidney, testes, spleen) Skin Blood, etc Skeleton The oxygen consumption of the different tissues can be calculated approximately from Tables IV. and V. For a frog of 100 grams weight the oxygen consumption per hour would be: Whole frog Skeletal muscle Plain muscle. Heart 5 c.c. 63x0O017=1-07 c.c. 4 x c.c.. 04x0 8 =032 c.c. It is interesting to note that in the resting animal the oxygen consumption of plain muscle is approximately equal to that of skeletal muscle. The skeletal, plain and cardiac muscle only account for half the resting oxygen consumption. The remainder presumably is accounted for by the respiratory and cardiac movements and by the central nervous system, glands and skin. SUMMARY AND CONCLUSIONS. 1. Stretching of the frog's bladder has no certain effect on its oxygen consumption.
6 186 Influence of Resting Length on the Oxygen Use of Plain Muscle 2. The oxygen consumption of plain muscle at rest is much higher than that of resting skeletal muiscle. 3. In a frog at rest the total oxygen consumption of the plain muscle is nearlv equal to the total oxygen consumption of the skeletal muscle. I am grateful to Professor CLARK for suggesting this work and for his constant help. REFERENCES. (1) EVANS, C. L., Journ. Physiol., 1923, lviii. 22. (2) PARNAS, Arch. f. d. ges. Physiol., 1910, cxxxiv (3) CLARK, A. J., and A. C. WHITE, Journ. Physiol., 1930, lxviii (4) WARBURG, Biochem. Zeitschr., 1923, cxlii (5) DAVID, J. C., " The action of oestrin on the oxygen consumption of the mouse's uterus," Journ. Pharm. and Exper. Therap. (In press.) (6) HILL, A. V., Proc. Royal Soc., B, 1929, civ. 39. (7) MEYERHOF and MEIER, Pfluiger's Archiv, 1924, cciv (8) MEYERHOF, Die chemischen Vorgiinge im Muskel, Berlin, 1930, p. 12. (9) FENN, W. O., Amer. Journ. Phvsiol., lxxxiv. 110.
junction with the great veins and the auricles removed. As much as 6I2.I73.0I9.76:6I2.26
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