intramuscularly per kilo weight). (c) The fowl was supine and part of the trachea was freed. The trachea
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1 525 J. Physiol. (1940) 97, I2.288:598.6 RESPIRATORY REFLEXES IN THE FOWL BY J. D. P. GRAHAM From the Institute of Physiology, University of Glasgow (Received 31 October, 1939) HERING & BREUER [1868] described the respiratory reflex in mammals whereby the stimulation of alternate inflation and deflation of the lungs gives rise to impulses in the vagi which result in the inhibition of inspiration and expiration. In this way the respiratory rate is kept automatically at an accelerated rhythm. This work was confirmed by Loewy [1888] and Head [1889] and the final links in the chain of evidence were supplied by Adrian [1933] and Gaylor [1934]. Further, Lumsden [1924] described a reflex in the mammal whereby the passage of a stream of air in the trachea initiated a series of impulses which cut short respiration in a manner closely resembling the Hering- Breuer reflex. The present paper gives details of an investigation into the presence and mode of working of these reflexes in birds, as represented by the fowl. METHODS The presence of the Hering-Breuer reflex was investigated by the following methods in the fowl anaesthetized with nembutal (0.75 grains intramuscularly per kilo weight). (a) The fowl was laid supine and the vagus nerves isolated. Respiration was recorded with a stethographic lever [Bell & Smellie, 1933]. Both vagi were cut. (b) With the fowl supine one vagus nerve was isolated. Respiration was recorded by a stethographic lever. The isolated vagus was then cut. The central end was stimulated with various strengths of induced current. Several preparations were used so that the effect of cutting the left and right vagus could be determined. (c) The fowl was supine and part of the trachea was freed. The trachea was clamped at full inspiration or at full expiration and the effect noted. (d) The thorax was opened and the right mesobronchus clamped. The thorax was then closed. This technique has been more fully described
2 526 J. D. P. GRAHAM [Graham, 1940]. The respiration was recorded by a stethographic lever. A hollow needle (a lumbar puncture needle of 14 mm. diameter) was thrust into the right abdominal air-sac. The needle was attached by pressure tubing to a recording mercury manometer arranged to write on the kymograph below the stethographic lever, and to a hand pump. By this procedure the right lung and its appendages, the air-sacs, were isolated with their nerve supply intact, and the air within them stabilized Fig. 1. Diagram of upper respiratory tract of fowl, showing cannulae in position for investigation of tracheal reflex. at atmospheric pressure. The pressure was increased by pumping or reduced by applying suction and the effect on respiration recorded, together with the altered pressure level. The experiment was modified by section of the right vagus nerve or of both vagi. (e) The tracheal reflex described by Lumsden [1924] was investigated by isolating as long a portion of the trachea as possible, and inserting three cannulae into it in the manner shown in Fig. 1. The cannula placed low down in the neck (Fig. 1) served for the continuance of respiration, which was recorded by a stethograph level applied to the carina. Of the
3 RESPIRATORY REFLEXES IN THE FOWL 527 other two cannulae, one was placed as high up as possible, facing caudad, the other was put as low down as possible, facing away from the lungs (craniad). A hand pump could be attached to either of these cannulae in order to send a stream of air along the isolated portion of trachea to imitate the inspiratory or expiratory flow. The duration of passage of such an air stream was recorded by a signal lever on the kymograph. This experiment was modified by single or double vagotomy and by the application of a local anaesthetic to the mucous membrane of the trachea. RESULTS (a) Respiration in the anaesthetized fowl is regular in rate and rhythm. Severance of the trunks of the vagi in the neck, after a short C. Normal breathing. A. 2 mi. after section of both vagi in the neck. B.2I 8 kg., anaesthetic and record asi above. Effect of stimulation of central end of cut right vagus, left vagus intact, induction coil at 20 cm. period of increased inspiratory tonus, slows the rate of respiration from 44 to 18 per min. (average of ten experiments), and increases the depth of respiration as judged by the stethograph. This alteration of the rate and rhythm is clearly sieen in Fig. 2 A. (b) The effect of section of one vagus nerve in the neck is to render the respiration somewhat irregular and slow. Stimuilation by induced currents of the central end of either vagus nerve, with the other nerve intact, produces slowing of the respiratory movements, increased in-
4 528 J. D. P. GRAHAM spiratory tonus and prolongation of expiration (see Fig. 2B). Stronger stimulation tends to cause increased inspiratory tonus with dyspnoea and convulsions. (c) If the respiratory movements be recorded on a fast drum the effect of occluding the trachea at the end of inspiration or expiration is as follows. In either case clamping of the trachea affects the next respiration. If the trachea be clamped at the height of inspiration this is followed by a short but definite pause before the next inspiration. If the trachea be clamped at the end of expiration the next inspiration follows at once. These phenomena are illustrated in Fig. 3 (A, B), which Fig. 3. Fowl, 2-0 kg., nembutal 0-75 grains per kg. intramuscularly. Respiratory record taken by stethograph lever. Read from left to right, inspiration upwards. A. Effect of clamping trachea at full inspiration (marked ).B. Effect of clamping trachea at full expiration (marked t ). may be compared with Fig. 477 in the current edition of Starling's Physiology [Evans, 1936]. There is no evidence of an increase in the height of inspiration following clamping of the trachea, as in the mammal. (d) The anaesthetized fowl is able to maintain satisfactory respiration after clamping the right mesobronchus. The rate is considerably increased and the amplitude diminished. The respiratory movements are regular in rate and rhythm. On inflating the lung and air-sacs on the right side the carina is raised by the filling of the thoracic and interclavicular airsacs. This effect modifies the record of respiration, giving a fallacious impression of increased inspiratory tonus. Superimposed upon this alteration in the respiratory record is the true effect of increased pressure in the lung, viz, marked expiratory effort followed by inhibition of respiration as a whole. This effect is shown in Fig. 4A. In this preparation, section of the right vagus nerve in the neck, or of both vagi, abolishes this expiratory effort and respiration assumes the slow rhythm seen after vagotomy. The mechanical raising of the carina is unaffectedl. The application of suction to the isolated lung system has no effect on respiration. The form of the record resulting from mechanical distension
5 RESPIRATORY REFLEXES IN THE FOWL 529 of the lung system in which the bronchus has been clipped is seen in Fig. 4B, where the pressure in the right lung has been increased after death. This record may-be taken as a base line when considering the alteration in respiration due-to changes in pressure in the lung and air-sacs. Fig. 4. Fowl 2*5 kg., nembutal 0-75 grains per kg. intramuscularly. Right mesobronchus clamped. Upper record respiration recorded by stethograph lever; lower record pressure in right lung and air-sacs in mm. Hg. Read from left to right, inspiration upwards. A. Effect of raising pressure in isolated lung system. B. Effect of raising pressure in same lung system after death. (e) If the respiratory movements in an anaesthetized fowl be recorded and the inspiratory air-stream be imitated according to the method described above [Fig. 1, p. 526], the rate of respiration is quickened to a slight degree, but the respiratory movements otherwise remain regular (Fig. 5 B). If the stream of air be reversed, as in expiration, the respiratory rate is slowed and expiration prolonged. The expiratory tonus may be increased and if the artificial expiratory stream is begun during inspiration, that inspiration is inhibited markedly (Fig. 5A). If the mucous membrane lining the isolated portion of trachea be swabbed with 2 % Decicaine solution, after 5 min. this reflex prolongation of expiration cannot be elicited. The reflex returns after 1 or 2 hr. when the effect of the local anaesthetic has worn off. Careful stripping of all connective tissue from the outer surface of the isolated portion of trachea severs it from its nervous connexions, and also destroys the reflex. The nerve
6 530 J. D. P. GRAHAM supply to the _imm trachea of the fowl is from the right and left vagus nerves. Section of the vagi in the neck above the level of the upper tracheal opening abolishes the reflex. Fig. 5. Fowl, 1-8 kg., nembutal 075 grains per kg. intramuscularly. Record of respiration by stethograph lever after triple tracheotomy (see Fig. 1). Read from left to right, inspiration upwards. A. Effect of expiratory air stream in trachea. B. Effect of inspiratory air stream in trachea. Note division of a normal respiratory movement into inspiratory and expiratory phases. DIsCUSSION That the Hering-Breuer reflex plays a fundamental part in the regulation of respiration in mammals has long been recognized. The various methods of investigating the reflex are set out in the series of classical papers mentioned above. The evidence which has accrued during the present work clearly shows that the Hering-Breuer reflex is present and operates in the fowl. The evidence for this may be briefly recapitulated thus. Section of the vagus nerve slows respiration (after the classical initial stimulation). Impulses which give rise to acceleration of respiration must therefore pass in the vagi. Stimulation of the central end of a cut vagus, the other nerve being intact, may give rise to increased inspiratory tonus or to prolongation of respiration. This reveals the probable nature of the impulses relating to respiration which pass up the vagus nerve. Low air pressure within the lungs, produced by clamping of the trachea at the end of expiration, induces immediate inspiration. Inflation of the isolated lung and air-sacs on one side induces an increased expiratory effort, which, on failure to reduce the intrapulmonary tension, is followed by inhibition of respiration as a whole. Section of the vagus nerves abolishes this effect. From these facts it is inferred that expansion of the avian lungs and air-sacs on inspiration gives rise to a series of impulses which pass up the vagi and cause the inspiration to be cut sbort. Similarly collapse of the lungs and air-sacs on expiration causes impulses to pass up the vagi which cut short expiration. This is the "Hering-Breuer reflex". It has been held [Thomson, 1923] that in birds inspiration is a passive act following upon forcible expiration. Examina-
7 RESPIRATORY REFLEXES IN THE FOWL 531 tion of the form of the stethographic record of respiration in the anaesthetized fowl lying supine shows that under these circumstances this is not so (see Fig. 5). The lever rises sharply on inspiration and falls slowly on expiration. It is interesting to compare this with the post-mortem record of Fig. 4 B. Here the lever rose sharply on inspiration produced by positive ventilation (active), and fell slowly on expiration produced passively by release of the valve of the pump. In mammals the expiratory impulses in the vagi started by inspiration play a more prominent part in the regulation of respiration than do the inspiratory impulses. This is so in the fowl as positive ventilation results in expiratory effort, while negative ventilation has no effect on respiration; in the experiment where the trachea was clamped, inflation of the lung and air-sacs (full inspiration) had more effect on the respiratory rhythm than deflation of the lung (full expiration). From the experiments where a stream of air was directed along the trachea while the anaesthetized fowl breathed through a separate tracheotomy tube, it is evident that we have here a reflex peculiar to birds and distinct from Lumsden's variety of the Hering-Breuer reflex. Blowing air along the trachea in the direction of inspiration has no effect on respiration, but blowing air along the trachea in the direction of expiration markedly inhibits inspiration. This is abolished by high section of the vagi nerves or cocainizing of the mucous membrane of the trachea. It is concluded, therefore, that we have here a reflex action by which expiration, once begun, is continued. In the fowl, therefore, inspiration begins, presumably as a result of increasing carbon dioxide tension in the blood. Distension of the lungs and air-sacs as a result of inspiration acts as a stimulus for the first part of the Hering-Breuer reflex whereby inspiration is inhibited. Expiration begins, largely as a passive movement (in the fowl placed on its back), and the passage of the expired air up the trachea promotes expiration, which continues as a forceful act. That portion of the Hering-Breuer reflex whereby expiration automatically promotes inspiration is weak. Expiration presumably ceases with alteration of blood ph. The unusual feature whereby we find two powerful reflexes inhibiting inspiration and promoting expiration may conjecturally be related to the function of flight in birds and to the peculiarities of respiration during ffight, or to the fact that the flow of air during inspiration is an unobstructed one from the trachea to the air-sacs via the main bronchi, while the air stream during expiration must meet with considerable obstruction in its passage through the recurrent bronchi and the fine parabronchial air capillaries
8 532 J. D. P. GRAHAM where gaseous exchange takes place [Graham, 1940]. Examination of a normal record of respiration shows that expiration lasts twice as long as inspiration (Fig. 5B). SUMMARY 1. Section of the vagus nerves in the neck of the anaesthetized fowl slows the respiratory movements (after initial stimulation). 2. Stimulation of the central end of one cut vagus with a weak induced current (the other vagus being intact) slows respiration and increases inspiratory tonus. 3. Clamping of the trachea after expiration promotes inspiration and vice versa. 4. Inflation of the isolated lung and air-sacs on one side promotes expiratory movements; deflation of the lung has no effect on respiration. 5. Blowing air in an expiratory manner along the trachea (in situ but separate from the lungs) inhibits inspiration. This effect is abolished by section of the vagi or cocainizing the mucous membrane of the trachea. An inspiratory air stream has no effect. 6. The Hering-Breuer reflex is present in the fowl in a modified form. The action of this reflex is chiefly to promote expiration. 7. Once begun expiration is continued by an expiratory reflex evoked by the passage of air out through the trachea. 8. Normally the expiratory phase of a respiratory movement lasts twice as long as the inspiratory phase. 9. These facts may be related to the differences in the direction of the flow of air during inspiration and expiration in the fowl. This work was aided by a grant from the Medical Research Council. REFERENCES Adrian, E. D. [1933]. J. Physiol. 79, 332. Bell, J. R. & Smellie, A. R. [1933]. J. 8Ci. Instrum. 10, 359. Evans, C. L. [1936]. Starling's Principles of Human Physiology, 7th ed. London: Churchill. Gaylor, J. B. [1934]. Brain, 57, 143. Graham, J. D. P. [1940]. J. Physiol. (in the Press). Head, H. [1889]. J. Physiol. 10, 1. Hering & Breuer [1868]. Sitz. Wien. Akad. Math. Nat. (2), 57, 672. Loewy, A. [1888]. P.fitg. Arch. ges. Physiol. 42, 273. Lumsden, T. [1924]. J. Physiol. 58, 111. Thomson, J. A. [1923]. Biology of Birds, p London: Sidgwick and Jackson. CAMBRIDGE: PRITED BY WALTER LEWIS, M.A., AT THE UNIVERSITY PRESS
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