[Gaskell, 1880] produced vaso-dilatation of muscle, and in a concentration
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1 6I i DOES MUSCULAR CONTRACTION AFFECT THE LOCAL BLOOD SUPPLY IN THE ABSENCE OF LACTIC ACID FORMATION? BY TSANG-G. NI. (From the Laboratory of Zoophysiology, University of Copenhagen.) IT is generally believed that the increased flow of blood to -active muscles is brought about by the increased formation of acid metabolites. Previous workers reported that lactic acid in a concentration of 1/10,000 [Gaskell, 1880] produced vaso-dilatation of muscle, and in a concentration of 0-05 to 0.01 p.c. [Anrep, 1912] caused hypereamia of the rabbit's ear. Fleisch [1921] pointed out that in almost all the perfusion experiments made prior to his report, the acid concentrations employed were many times higher than could occur in living tissue. He therefore used perfusion fluids of low concentration of acid, and found that even a slight increase in the hydrogen ion concentration induced a distinct increase in the volume perfused. On the other hand, recent work [Krogh, 1929] showed that buffer mixtures of ph = 3x65 to ph = 2*96 applied to the ventral surface of the frog's tongue gave no, or doubtful, dilatation, and that a mixture of 10 p.c. C02 in air produced no widening of capillaries. The difficulty hitherto encountered was that muscular contraction was inseparably bound up with increased formation of acids. What all the previous authors on this problem tended to examine was whether acid-without contraction-alone would play a part in the peripheral regulation of the blood supply. It is therefore highly desirable to attack the problem from another angle, that is, whether contraction-without increase in lactic acid-alone would affect the supply of blood to the stimulated muscle. The physiological significance of an increase in blood supply to an active muscle is to facilitate the exchange of substances between the blood and the tissues whichtakes place in the capillaries. The conditions of supply are affected by a dilatation of arterioles which increases the flow of blood, and by a dilatation and opening up of capillaries which increase
2 BLOOD SUPPLY TO MUSCLES. the surface area available for the exchange of substances and shorten the distances through which they have to be transported. In the present report I have disregarded the flow and applied the methods for studying capillaries, chiefly by counting. METHODS. To prevent the increase in lactic acid caused by muscular contraction, the procedure described by Lundsgaard [1930] was followed. Frogs were used. In all cases, unless otherwise mentioned, transection of the spinal cord below the medulla was performed at least one day before each experiment was done. Voluntary movements were thus abolished, while the nerves to the hind legs were uninjured. Fifty minutes after the injection of monoiodoacetic acid, 01 mg. per g. of body weight, into the dorsal lymph sac, the anterior tibial muscle (m. tibialis anticus longus), sometimes the gastrocnemius and, in a few cases, the thigh muscles of one side were stimulated by induced currents (a locally made inductorium, secondary coil at 6 cm.). After seventy separate shocks at the rate of one per 2 seconds, with intervals for rest, had been given, a graphite suspension [Drinker and Churchill, 1927] was introduced slowly by intracardial injection. The graphite was thus distributed through the action of the heart to the vessels in use-vessels which were already patent. For my present work the concentration of the suspension used was between "5 and 10'" as estimated according to the technique recommended by Perry [1930]. Five to eight minutes after the injection of graphite, both the stimulated and the control side were removed and prepared for imbedding, cutting and finally for counting of capillaries in the injected preparations. The counting of the number of open capillaries was made on transverse sections. Averages of five to six countings, each made on an area of sq. mm., were taken. RESULTS. Although it was shown by a previous author [Krogh, 1919] that capillaries are distributed among the muscle fibres with conspicuous regularity, only a great difference in the number of capillaries between the stimulated and the control muscles was taken as significant for reasons to be discussed later. When the injected muscles were fixed, dehydrated and rendered PH. LXXI
3 358 TSANG-G. NI. transparent by means of soaking them in wintergreen oil, one could clearly see with unaided eyes the marked difference in the number of injected vessels between the stimulated and the control resting muscles. In the resting muscles of the control side only a few "black threads" (injected vessels) were seen running inside the transparent muscle tissue; in the stimulated muscles of the other leg a very great number of vessels were injected. When such vitally injected legs were so arranged and covered with wintergreen oil in a glass chamber that a photograph could be taken by transmitted light, the photograph showed in the resting side some injected vessels running in the transparent tissues, while in Fig. 1. A, control side; B, stimulated side. the stimulated side the -injected vessels were so nulmerous that they gave the thigh muscles especially the appearance of a black mass. By counting the number of open capillaries, however, at corresponding levels of stimulated and control muscles, quantitative and more accurate information was obtained. The results presented in Table I were obtained from preparations of m. tibialis anticus longus with the exception of Exp. 5, in which the gastrocnemius muscles were employed. Although the increase in the lactic acid was prevented in such cases, the local blood supply after contraction was undoubtedly increased as evidenced by the number of open capillaries. The number of patent capillaries in stimulated muscles
4 BLOOD SUPPLY TO MUSCLES. 359 ranged from 139 to 198 per sq. mm.; in corresponding muscles of the resting side there were very few. The highest increase was thirty-ninefold (Exp. 14). When the dose of monoiodoacetic acid was large (0.4 mg. per g.), stagnation of circulation took place very soon; both the local stasis and the rigor of the muscles occurred earlier in the stimulated side than in the control leg. Consequently, in such cases, the stimulated muscles showed only a few injected capillaries (Exp. C). In a case in which the sciatic nerves were cut instead of transection of spinal cord, fairly good numbers of injected capillaries were found in both the active and the control muscles. This might be due to the loss of the sympathetic influence in the maintenance of the normal tonus of local vessels. TABLE I. Number of patent capillaries per sq. mm. from averages of five to six countings. Control Control Experiments Stimulated (resting) Experiments Stimulated (resting) 1* * * * * * C * * Muscles of left leg were stimulated; in other oases those of right leg were stimulated. DISCUSSION. In longitudinal sections it was noted that in some parts capillaries appeared as continuous black lines, in other parts they are interposed by black dots. Apparently in vital injections the replacement of blood by graphite was not always complete. It was necessary therefore to make enough allowance for errors caused by such uneven distribution of the graphite. Countings made on sections cut at various levels showed that the deviation from the mean was usually less than 40 p.c. The increase in patent capillaries after contraction was as much as seven- to thirtynine-fold. As already mentioned, large doses of monoiodoacetic acid would produce stagnation of circulation. For the purpose of vital injection it was our practice to avoid anything which would cause stagnation. The results presented in Table I were taken from cases under the influence of a small amount (0.1 mg. per g.) of monoiodoacetic acid. The question was whether such a quantity might be insufficient to prevent the forma- 24-2
5 360 TSANG-G. NI. tion of lactic acid. This was answered by the following experiments. 0.1 mg. per g. of monoiodoacetic acid was injected into two series of frogs (transections of the spinal cord were made on a previous day). In one series muscles were stimulated by separate shocks under the conditions described above. The muscles were then prepared for the estimation of lactic acid according to the zinc lactate method [Fletcher and Hopkins, 1906]. In the other series the muscles were not stimulated. In the stimulated series the lactic acid found was 0*021 mg. p.c.; in the control series, mg. p.c. The present results tend to show that, in the absence of increase in lactic acid, muscular contraction can still promote the local supply of blood by opening up more capillaries. In connection with the two important factors: (a) the available capillary surface, and (b) the rate of blood flow, most previous authors have emphasized (b); the present work has been planned to deal with (a). Our results, however, do not exclude the possibility that lactic acid might play some part in the regulation of the rate through its action on the cardio-vascular system other than the capillaries. Although stimuli were directly applied to the leg, the possibility of the spreading of current to nerves was not excluded. Indeed in all cases the reflex arc was not destroyed, and it was impossible to be certain just how much could be attributed to the mechanical effect of the contraction and how much to the nervous influence. According to Krogh, stimulation of the nerve to a muscle fails to cause any opening up of capillaries, when contraction is prevented by curare, but a reflex relaxation of sympathetic tone is an obvious possibility in voluntary or reflex contractions. In the present series I tried to ascertain the influence of nerve stimulation when the muscular contraction was prevented by curare. The curare we had on hand produced stagnation of the circulation even before the motor endings had been completely paralysed, and consequently the vital injection in this curare series was unsuccessful. "Antidromic reaction" [Bayliss, 1901; Doi, 1920; Krogh, Harrop and Rehberg, 1922] was not sufficient to account for the present results, since stimulation of posterior roots did not increase the number of patent capillaries beyond the experimental error. Krogh [1929] reported that a mixture of 10 p.c. of CO2 in air, a tension so high that it probably never occurs in normal frogs, produces an increase in circulation in a few capillaries, but the general increase over the whole field was too slight to be ascertained. Since in the present work the blood circulation was going on until the removal of the legs,
6 BLOOD SUPPLY TO MUSCLES. 361 there could not be much accumulation of CO2 in the muscle. My results, however, do not preclude the possibility of the formation of active substances other than lactic acid. For instance, stimulation might liberate from the cell protein some "dilator hormone," comparable to the formation of H-substances [Lewis and Grant, 1924] in stimulated mammalian tissues. SUMMARY. When the formation of lactic acid is prevented by poisoning with monoiodoacetic acid, muscular contraction can still increase the local blood supply by opening up more capillaries. Evidently lactic acid from the muscle is not an essential part of the mechanism which regulates the peripheral blood flow. Whether a humoral intervention of a substance other than lactic acid exists, is not discussed. It is a great pleasure to express my thanks to Prof. Krogh and to Dr Re hb erg for the laboratory facilities and for their counsel; to Prof. Lindhard for the privilege of using his microtome, and to Mr Lange for taking the photograph. REFERENCES. v. Anrep, G. ( ). J. Physiol. 45, 318. Bayliss, W. M. (1901). J. Phy8iol. 26, 173. Doi, Y. (1920). J. Physiol. 54, 227. Drinker, C. H. and Churchill, E. D. (1927). Proc. Roy. Soc. B, 101, 462. Fleisch, A. (1921). Z. allg. Phy8iol. 19, 269. Fletcher, W. M. and Hopkins, F. G. (1906-7). J. Phy8iol. 35, 247. Gaskell, W. H. ( ). J. Phy8iol. 3, 48. Krogh, A. (1919). J. Physiol. 52, 405. Krogh, A. (1929). Anatomy and Physiology of Capillaries. New Haven, 2nd ed., pp , 257. Krogh, A., Harrop, G. A. and Rehberg, P. B. (1922). J. Physiol. 56, 179. Lewis, T. and Grant, R. T. (1924). Heart, 11, 209. Lundsgaard, C. (1930). Biochem. Z. 217, 162. Perry, I. H. (1930). Skand. Arch. Physiol. 59, 67.
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