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Breathing and the Control of Heart Rate Erica Potter BREATHING AND THE CONTROL OF HEART RATE by ERICA POTTER School of Physiology and Pharmacology University of New South Wales . : '.,; ' Ph.D . January 1981 ACKNOWLEDGEMENTS I am very grateful to Professor W.E Glover for enabling me to undertake this project in the School of Physiology and Pharmacology, to the National Heart Foundation of Australia for its support of this project, to Miss Diane Madden for her untiring technical help, to Dr. Simon Gandevia for a stimulating period of collaboration, to Mrs. Judy Bokor who typed this thesis and especially to my supervisor, Associate Professor Ian Mccloskey for his encouragement, pa~ience and guidance throughout. STATEMENT REGARDING WORK DONE IN COLLABORATION Some of the results reported in chapter 3 have been published in a paper (Davis, Mccloskey and Potter, 1977) whicl included also some results from work done by Dr. Anne Davis. Dr. Davis and I did not perform our experiments together, and none of her results are included in this thesis. Experiments involving recordings of heart rate in animals and man are described in chapters 4, 5 and 6; some of these were performed in equal collaboration with Dr. Simon Gandevia and were published with him (Gandevia, McCloskey and Potter, 1978 a, b). The collaborative work done with Dr. Gandevia was not included in his Ph.D thesis. The experiments on nerve recordings in the same chapters and elsewhere throughout this thesis were performed by me. Associate Professor Ian Mccloskey supervised my work and collaborated in many experiments. PUBLICATIONS ARISING FROM WORK DESCRIBED IN THIS THESIS 1. Davis, A.L., Mccloskey, D.I, and Potter, E.K (1977). Respiratory modulation of baroreceptor and chemo­ receptor reflexes affecting heart rate through the sympathetic nervous system. J .Physiol. 272 : 691 - 70: 2. Gandevia, S.C., McCloskey, D.I, and Potter, E.K (1978). Inhibition of baroreceptor and chemoreceptor reflexes on heart rate by afferents from the lungs. J. Physiol. 276 : 369 - 381. 3. Gandevia, S.C., Mccloskey, D.I, and Potter, E.K (1978). Reflex bradycardia occurring in response to diving, nasopharyngeal stimulation and ocular pressure, and its modification by respiration and swallowing. J. Physiol. 276 : 383 - 394. 4. McCloskey, D.I, and Potter, E.K (1981). Excitation and inhibition of cardiac vagal moto­ neurones by electrical stimulation of the carotid sinus nerve. J.Physiol. in press. 5. Potter, E.K (1981). Inspiratory inhibition of vagal responses to baro­ receptor and chemoreceptor stimuli in the dog. J. Physiol. in press. 1 TABLE OF CONTENTS Page TABLE OF CONTENTS 1 ABSTRACT 5 CHAPTER 1 INTRODUCTION (5 figs) 8 1. GENERAL INTRODUCTION 9 2. ACTIONS OF THE VAGUS 9 3. ANATOMY 11 (a) Cardiac vagal preganglionic 11 neurones (b) Properties of cardiac vagal 13 fibres (c) Afferent pathways 15 4. REFLEXES THAT EXCITE THE VAGUS 18 (a) Baroreceptor reflex 18 (b) Chemoreceptor reflex 23 (c) Diving response 25 (d) Oculocardiac and other 27 reflexes (e) Ventricular receptors 28 (f) Juxtapulmonary capillary 29 receptors (g) Vasovagal syncope 31 5. SINUS ARRHYTHMIA 32 6. RESPIRATORY MODIFICATIONS OF 35 REFLEXES (a) Carotid sinus nerve 35 stimulation (b) Functional stimulation 39 2 Page 7. EXPERIMENTAL CONSIDERATIONS 42 (a) Identification of cervical 42 cardiac vagal efferent fibres (b) Effects of anaesthesia 43 CHAPTER 2 METHODS (2 figs) 47 1. WHOLE ANIMAL EXPERIMENTS WITH 48 OBSERVATIONS ON HEART RATE 2. NERVE RECORDING EXPERIMENTS 52 3. HUMAN EXPERIMENTS 59 CHAPTER 3 RESPIRATORY MODULATION OF BARO­ 61 RECEPTOR AND CHEMORECEPTOR REFLEXES MEDIATED BY THE VAGUS AND THE SYMPATHETIC NERVOUS SYSTEM (6 figs) 1. VAGAL RESPONSES 62 2. SYMPATHETIC EFFECTS 64 (a) Baroreceptor responses 66 (b) Chemoreceptor responses 69 3. DISCUSSION 71 CHAPTER 4 CENTRAL AND PERIPHERAL FACTORS 76 MODIFYING BARORECEPTOR AND CHEMORECEPTOR REFLEXES (11 figs) 1. CENTRAL MODULATION OF REFLEX 77 RESPONSIVENESS 2. PERIPHERAL MODULATION OF 81 REFLEX RESPONSIVENESS (a) Effects of stimuli timed with 81 respect to air flow into the lungs · fast ramps (b) Effects of stimuli timed with 85 respect to air flow into the lungs slow ramps (c) Effects of denervation of 88 the lungs 3. DISCUSSION 98 3 Page CHAPTER 5 RESPIRATORY MODULATION OF OCULOCARDIAC 104 AND NASOPHARYNGEAL REFLEXES (5 figs) 1. OCULOCARDIAC REFLEX 105 2. NASOPHARYNGEAL STIMULATION 111 3. DISCUSSION 113 (a) Oculocardiac reflex 113 {b) Diving reflex 115 CHAPTER 6 RESPIRATORY MODULATION OF CARDIO­ 116 DEPRESSOR REFLEXES IN NORMAL HUMAN SUBJECTS . (4 figs) 1. OCULOCARDIAC REFLEX 118 2. DIVING RESPONSE 121 3. BREATH HOLDING IN NORMOXIC 121 AND HYPOXIC CONDITIONS 4. DISCUSSION 124 CHAPTER 7 ANALYSIS OF MECHANISMS OF 127 INSPIRATORY INHIBITION OF VAGAL ACTIVITY (8 figs) 1. RESPIRATORY EFFECTS OF VAGAL 129 TONE 2. PROPERTIES OF THE VAGAL 133 INHIBITORY PATHWAY (a) Interactions with central 133 inspiratory activity (b) Interac~ions with effects 137 from lung inflation 3. DISCUSSION 140 CHAPTER 8 COMPARISON OF VAGAL RESPONSES TO 149 ELECTRICAL STIMULATION OF THE CAROTID SINUS NERVE AND TO BRIEF BARORECEPTOR STIMULI (13 figs) 1. RESPONSES EVOKED BY SINGI.;E 150 ELECTRICAL STIMULI TO THE CAROTID SINUS NERVE (a) Variability of response 150 latencies 4 Page (b) Respiratory modulation of 151 variability of response latencies (c) Inhibition of vagal discharge 156 following responses elicited by single electrical stimuli 2. RESPONSES EVOKED BY MULTIPLE 165 STIMULI TO THE CAROTID SINUS NERVE (a) Vagal responses to pairs of 165 electrical stimuli (b) Vagal responses to trains of 165 electrical stimuli 3. RESPONSES TO BRIEF BARORECEPTOR 167 STIMULI (a) Single stimuli 167 (b) Pairs of baroreceptor stimuli 169 4. DISCUSSION 173 CHAPTER 9 GENERAL DISCUSSION (3 figs) 180 1. PHENOMENA STUDIED 181 2. METHODS 182 3. MECHANISMS 187 4. SIGNIFICANCE 192 5. APPLICATIONS 195 6. FURTHER EXPERIMENTS 196 REFERENCES 198 5 ABSTRACT Heart rate alters with breathing. The neural basis of the relationship between the two was studied in the experiments described in this thesis. There are several reflexes that slow the heart. Four were studied in detail here: the baroreceptor reflex, the chemoreceptor reflex, the diving response and the oculo­ cardiac reflex. The heart can be slowed by activation of cardiac vagal nerves or by withdrawal of cardiac sympathetic activity the sympathetic contribution to the slowing of the heart is relatively smaller and slower. Heart rate was studied in anaesthetised dogs and conscious human subjects. Dogs were chosen as experimental animals because even when anaesthetised they maintain a high level of cardiac vagal tone. More quantitative aspects of the interaction of breathing with the neural control of heart rate were studied in anaesthetised dogs by recording activity in single vagal efferent nerve fibres running to the heart. It has been shown here that each of the reflexes studied can slow the heart only, or most effectively, in the expiratory phase of breathing. The bradycardia evoked by selective stimulation of these reflexes during expiration is due both to vagal excitation and sympathetic withdrawal. Selective stimulation of any one of these reflexes is inhibited in inspiration. This inspiratory inhibition has 6 two components a peripheral one caused by activation of intrapulmonary receptors stimulated during lung inflation, and a central one related to the cyclical activity of inspiratory neurones. Lung inflation alone, in the absence of central inspiratory activity can inhibit these reflexes, or central inspiratory activity alone in the absence of lung movements can also inhibit these reflexes. Nerve fibre recordings in anaesthetised dogs showed differences in the mechanisms of inspiratory inhibition caused by lung inflation and central inspiratory activity. Selective stimulation of arterial baroreceptors or chemo­ receptors was used to evoke reflex increases in vagal activity. Lung inflation inhibits reflexly-evoked increases in vagal discharge but leaves any resting vagal discharge relatively unaffected. Central inspiratory activity, on the other hand, inhibits both reflexly-evoked increases in vagal firing together with resting vagal discharge. These results are accommodated in two models of the vagal-excitatory pathway proposed in Chapter 7. Briefly, these models have lung inflation inhibiting the baroreceptor-afferent to vaga~-efferent pathway relatively early in that pathway, while central inspiratory activity has its inhibitory action relatively late in the reflex pathway. Electrical stimulation of the carotid sinus nerve was also used to study the central connectiomof baroreceptor and chemoreceptor reflexes. Although such stimulation is a 7 useful physiological tool in the investigation· of reflex pathways its excitatory action on the vagus differs in several important respects, documented here, from excitation caused by selective functional stimulation by baroreceptors and chemoreceptors. In conscious human subjects three cardiodepressor reflexes were tested: the oculocardiac reflex, the diving response and bradycardia evoked by hypoxia. Each of these reflexes is inhibited by inspiration. This confirms the results obtained in anaesthetised dogs and justifies the use of anaesthetised dogs as suitable animal models in which to study the interaction of breathing with heart rate. Central inspiratory activity alone was tested here in human subjects by having them swallow, or take an inspiratory effort-against a closed glotis (with, consequently, little accompanying lung expansion). Both these manoeuvres inhibited the reflexes
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