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Interactions Between Respiration and Circulation

M. De Burgh Daly

10.1002/cphy.cp030216

Source: Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Spontaneous Respiratory Variations in the Cardiovascular System
1.1 Arterial Blood Pressure
1.2 Heart Rate
1.3 Cardiac Output
1.4 Systemic Vascular Resistance
1.5 Pulmonary Hemodynamics
2 Central Nervous Control of Respiration and the Cardiovascular System
2.1 Receptors and Afferent Pathways
2.2 Cell Bodies and Efferent Pathways
2.3 Central Control of Sympathetic Efferent Activity
2.4 Descending Pathways to Spinal Sympathetic Outflow
3 Central and Local Peripheral Circulatory Control by Blood Gases
3.1 Central Effects
3.2 Peripheral Effects
4 Some Reflex Neural Control Mechanisms
4.1 Arterial Baroreceptors
4.2 Peripheral Arterial Chemoreceptors
4.3 Upper Airway Receptors
4.4 Facial Receptors
4.5 Cardiopulmonary Receptors
4.6 Overall Involvement of Cardiopulmonary Receptors
5 Reflex Cardiovascular Effects of Lung Inflation
5.1 Cardiac Responses
5.2 Changes in Systemic Vascular Resistance
5.3 Coronary Circulation
5.4 Nature of Pulmonary Receptors
6 Mechanisms of Respiratory Modulation
6.1 Pulmonary Vagal Reflex
6.2 Central Respiratory Neuronal Activity
6.3 Hypocapnia
7 Phasic Respiratory Modulation of Reflex Responses
7.1 Respiration
7.2 Heart Rate
8 Respiratory Modulation of Specific Inputs to Nervous System
8.1 Modulation by Hyperventilation
8.2 Modulation by Reflex Hypoventilation and Apnea
8.3 Interactions Between Carotid Baroreceptors and Chemoreceptors
9 Respiratory Modulation of Vagal and Sympathetic Efferent Fiber Activity
9.1 Activity in Cardiac Vagal Efferent Fibers
9.2 Activity in Sympathetic Efferent Nerves
9.3 Mechanisms of Central Integration
10 Respiratory Sinus Arrhythmia
10.1 Mechanisms
11 Some Examples of Respiratory‐Circulatory Integrative Control
11.1 Effects of Deep Breath
11.2 Valsalva Maneuver
11.3 Acute Hypoxia
11.4 Hypocapnia
11.5 Hypercapnia
11.6 Asphyxia and Breath Holding
11.7 Breath‐Hold Diving
12 Effects of Changes in the Cardiovascular System on Respiration
12.1 Respiration, Metabolism, and Cardiac Output
12.2 Hemorrhagic Hypotension
13 Medical Implications of Respiratory‐Cardiovascular Interactions
13.1 Diving Response
13.2 Protective Effects of Defense Mechanisms
13.3 Exaggerated Defense Responses
13.4 Restoration of Normal Cardiac Rhythm
13.5 Sudden Infant Death Syndrome
Figure 1. Figure 1.

Nervous control of respiratory and cardiovascular systems by arterial baroreceptors and chemoreceptors with some other inputs to nervous system by which integration between the 2 systems takes place. and arterial partial pressure of O2 and CO2, respectively.
Figure 2. Figure 2.

Sections of continuous tracing that show effects of changing respiratory rate on relationship between respiration and blood pressure in a human. During breathing, subject followed sinusoidal signal of slowly varying period. Between two slowest (top) and fastest (bottom) respiratory rates there is almost complete reversal of relation of blood pressure change to respiratory phase. Inspiration corresponds to downward movement of spirogram.

From Dornhorest et al. 227 by permission of the American Heart Association, Inc
Figure 3. Figure 3.

Effect of spontaneous respiration on venous return and cardiac output in dog with closed chest. Tracings from top to bottom: time and base line, aortic pressure (mmHg), pulmonary artery pressure, superior vena caval and intrathoracic pressures (mmH2O), pulmonary arterial and superior vena caval flows (ml · min−1). A, beginning of inspiration; S, acceleration of superior vena caval flow during ventricular systole; D, acceleration of superior vena caval flow during ventricular diastole. Stroke volume (ml) is shown below pulmonary arterial flow curve. Volume (ml) through superior vena cava during each cardiac cycle is shown at bottom. Electrical frequency response of both flowmeters is reduced from 400 to 40 Hz. Superior vena caval pressure curve is damped.

From Brecher 87. In: Venous Return, © 1956, Grune & Stratton
Figure 4. Figure 4.

Effects on heart rate and systemic vascular resistance of lung inflation during apneic asphyxia in dog with cardiopulmonary bypass, constant systemic blood flow, closed chest, and spontaneous respiration. Carotid sinus, aortic arch, and arterial blood = 138 mmHg, = 42 mmHg, and pH = 7.35. A: at signal, apneic asphyxia produced by reducing tidal volume of isolated perfused extracorporeal donor lungs from 400 to 75 ml while abolishing recipient's lung movements by injecting 3 mg of decamethonium into systemic arterial inflow tube. Break in record lasted 2 min. B: apneic asphyxia continued (carotid sinus, aortic arch, and arterial blood = 70 mmHg, = 71 mmHg, and pH = 7.19). Two maintained lung inflations with ∼300 ml air injected into trachea. Between B and C: tidal volume of isolated perfused lungs was restored to 400 ml. C: combined stimulation of carotid and aortic bodies by hypoxic hypercapnic blood ( = 40 mmHg, = 51 mmHg, and pH = 7.30). Systemic arterial blood = 130 mmHg, = 41 mmHg, and pH = 7.35. HR, heart (atrial) rate; TV, tidal volume (inspiration upward); AAP, mean aortic arch pressure; CSP, mean carotid sinus pressure; BP, mean systemic arterial perfusion pressure.

From Angell‐James and Daly 24
Figure 5. Figure 5.

Effects of maintained lung inflation with different pressures and volumes on systemic vascular resistance in 3 experiments. A and B: inflation volume and inflation pressure, respectively, are plotted against change in vascular resistance. Between inflations, lungs were allowed to collapse. C and D: same relationships are shown, but lungs were inflated from an expiratory pressure of 4 (○), 6 (•), and 10 (Δ) cmH2O. D: inflation pressure is difference between that at beginning and completion of inflation.

From Daly et al. 186
Figure 6. Figure 6.

A, B, and C: effects of stimulating carotid bodies with hypoxic blood in anesthetized dog on positive‐pressure artificial respiration with open pneumothorax. A and C: control states taken during normal artificial ventilation. Respiratory pump stroke volume = 150 ml, arterial blood = 38 mmHg, and pH = 7.35. B was taken 4 min after increasing stroke volume to 430 ml. Arterial blood = 24 mmHg and pH = 7.49. Frequency of pump was constant at 20 cycles · min−1. CSP, mean carotid sinus perfusion pressure; BP, mean systemic arterial blood pressure; HR, heart rate.

From Daly and Hazzledine 184
Figure 7. Figure 7.

Effects on heart rate of brief carotid body stimuli delivered during different phases of respiratory cycle in spontaneously breathing anesthetized dog. Records of tidal volume (inspiration upward), electrocardiogram (ECG), right atrial pressure (RAP), and arterial blood pressure (BP) are shown. A‐C: injections of CO2‐saline into carotid bifurcation caused brief chemoreceptor stimulation. When these stimuli were delivered during expiration (A and C), they evoked a prompt slowing of the heart and an expiratory effort. When stimuli were delivered during inspiration (B), they evoked an increased inspiratory effort but no change in heart rate. As control, chest was squeezed at D to mimic thoracic and atrial pressure changes seen with chemoreceptor stimuli given in expiration, but this did not affect heart rate.

From Haymet and McCloskey 323
Figure 8. Figure 8.

Modulation by phasic changes in respiration of respiratory and heart‐rate responses to brief stimuli applied to carotid body chemoreceptors by agents injected into common carotid artery. Stimuli were delivered to carotid bodies during inspiratory (○) and expiratory (•) phases of respiratory cycle. Ordinate: phase of respiratory cycle (inspiration, expiration), change in amplitude of inspiration, change in duration of expiration, or change in heart rate. Abscissa: time.

Data from Black and Torrance 81, Eldridge 250, Haymet and McCloskey 323, and M. de B. Daly (unpublished observations)
Figure 9. Figure 9.

Respiratory modulation of cardiac reflex responses to brief stimulations of carotid chemoreceptors and baroreceptors by 2 components, central inspiratory neuronal drive and pulmonary vagal reflex, in anesthetized animal paralyzed with neuromuscular blocking agent. Arrows, timing in relation to respiratory events of brief stimuli applied to carotid bodies (○) or carotid baroreceptors (•). Left: central inspiratory modulation alone; lungs were held in expiratory position to exclude pulmonary reflex component. Right: modulation by lung inflation during cessation of central inspiratory drive. (Compare arrow b with c, and c with d.) Note that lung denervation abolished modulation by lung inflation of chemoreceptor and baroreceptor responses.

Data from Daly and Angell‐James 178, Davidson et al. 203, and Gandevia et al. 273
Figure 10. Figure 10.

Effects of elective sustained stimulation of isolated perfused carotid body chemoreceptors by hypoxic hypercapnic blood on heart rate and respiration in spontaneously breathing animals. Relationship between changes in heart rate and respiratory minute volume under steady‐state conditions. •, Dog 193; ○, cat 191,486; x, seal 252; Δ, monkey 187.
Figure 11. Figure 11.

Reflex effects of lung inflation on vasoconstrictor responses elicited by stimulation of carotid bodies (CB) and aortic bodies (AB) in dog with cardiopulmonary bypass, constant systemic blood flow, open pneumothorax, and no ventilation of lungs. Separate perfusions of isolated carotid sinuses and of isolated aortic arch with blood from disk equilibrator ( = 140 mmHg, = 47 mmHg, and pH = 7.34). A‐D, effects of stimulation of CB and AB by hypoxic hypercapnic blood ( = 21 mmHg, = 83 mmHg and pH = 7.17) during continuous signal. Between arrows, lungs were inflated with 300 ml of room air. Between B and C, lungs were denervated. Note abolition of effects of lung inflation in C and D. At X, paper was stopped for 1.5 min. CSP, mean carotid sinus pressure; AAP, mean aortic arch pressure; BP, mean systemic arterial blood pressure. Time marker, 10 s.
Figure 12. Figure 12.

Central respiratory modulation of heart rate (HR) during stimulation of carotid body chemoreceptors in anesthetized dog with open chest and positive‐pressure ventilation. Both lungs are denervated by method of Daly and Scott 193. Av ENG, averaged phrenic electroneurogram; ENG, phrenic electroneurogram (efferent activity); ITP, intratracheal pressure; RM, rib movements (inspiration upward); BP, arterial blood pressure (mean and phasic). At signal, there was an intracarotid injection of 5 μg · kg−1 of sodium cyanide. Time marker, 10 s.

From Daly and Angell‐James 178
Figure 13. Figure 13.

Effects on changes in P‐P (P‐wave) interval of stimulating carotid baroreceptors (neck suction, −30 mmHg) for 0.6 s during early inspiration (left) and during expiration (right). Averaged P‐P intervals for 6 normal human subjects. •, Spontaneous changes provoked by inspiration without baroreceptor stimulation (0 mmHg); ▴, changes in pulse interval after neck suction applied in early inspiration; ▪, net response to baroreceptor stimulation (difference) calculated by subtracting responses without neck suction from responses with neck suction. TV, tidal volume

From Eckbere and Orshan 246
Figure 14. Figure 14.

Effects in 1 subject of single breath on cardiac response produced by stimulation of carotid sinus baroreceptors during period of apnea in expiratory position started 5 s earlier. Top: during apnea, 3 tests of baroreceptor stimulation started at zero time. In 2 tests (○, ▴), a single breath was taken, ↑, Start of inspiration; ↓, peak of inspiration and beginning of expiration. Bottom: 2 tests of apnea started at zero time. In one test (□), a single breath was superimposed as indicated by arrows. (J. E. Angell‐James and M. de B. Daly, unpublished observations.)
Figure 15. Figure 15.

Reflex interactions between inputs from trigeminal facial receptors (stimulated by water during experimental dive) and carotid body chemoreceptors. Effects of stimulating carotid body chemoreceptors alone [▪; (CB)] and during experimental dives [▪; (ED + CB)] on pulse interval and respiratory minute volume; experimental dives alone [□; (ED)]; control values [•; (C)]. Values are means ± SE from 10 tests in 5 animals. Where SE bars are not given, SE is less than size of symbol.

From Eisner et al. 252
Figure 16. Figure 16.

Effects of stimulating carotid body chemoreceptors with cyanide (7.0 μg · kg−1) alone and during period of apnea reflexly induced by electrical stimulation of central end of a superior laryngeal nerve in dog with intermittent positive‐pressure ventilation and open pneumothorax. A: superior laryngeal nerve stimulation (3V, 1 ms, 15 Hz). B: carotid body (CB) stimulation alone. C: carotid body stimulation during stimulation of superior laryngeal nerve. Repeat stimulation of carotid body alone (not shown) had effect similar to that shown in B. ITP, intratracheal pressure; RM, movements of the ribs (inspiration upward); BP, arterial blood pressure. Time calibration and time marker, 10 s.

From Angell‐James and Daly 31
Figure 17. Figure 17.

Three‐dimensional plot of relationship between time (t), pulse interval (PI) and volume (Vt) of right (test) lung (filled areas) during electrical stimulation of superior laryngeal nerve with stimulation of carotid body chemoreceptors by intracarotid cyanide in anesthetized dog with open pneumothorax. Tracheal divider separated left and right lung airways. Artificial ventilation of naturally perfused denervated left lung. Right lung was innervated, but pulmonary artery blood flow was obstructed by balloon. A: electrical stimulation of superior laryngeal nerve (bar) combined with intracarotid injection of cyanide at beginning of bar while right lung was in expiratory position (zero volume). B: right lung in expiratory position during combined stimulation of a superior laryngeal nerve and carotid body (bar) followed by inflation of right lung at arrow. Between B and C, right lung was denervated. C: inflation of right lung began at arrow during combined stimulation of superior laryngeal nerve and carotid body.

From Angell‐James and Daly 32
Figure 18. Figure 18.

Effects of stimulating carotid body chemoreceptors on carotid sinus baroreceptor control of muscle vascular resistance in 9 anesthetized, artificially ventilated, paralyzed, and vagotomized cats. Graphs show relationship between pressure in partly isolated perfused carotid sinuses and muscle vascular resistance (A) and arterial blood pressure (B). •—•, No carotid body stimulation; ○—○, with carotid body stimulation. C: carotid sinus pressure is related to the differences between the responses in A and B in terms of muscle vascular resistance (○) and arterial blood pressure (□), respectively, obtained at each carotid sinus pressure level with and without coexisting chemoreceptor stimulation. Values are means ± SE of numerous tests.

From Wennergren et al. 663
Figure 19. Figure 19.

Interactions between carotid baroreceptors and chemoreceptors in cat anesthetized with Althesin. A: response produced by inflating carotid blind sac to 210 mmHg. B: response evoked by stimulating carotid chemoreceptors with saline equilibrated with CO2 C: effect of stimulating chemoreceptors during an ongoing baroreceptor reflex. Resp., respiratory air flow; Vm, respiratory minute volume; HR, heart rate; BP, arterial blood pressure. In C, baroreceptor reflex was fully suppressed on chemoreceptor stimulation.

From Marshall 499
Figure 20. Figure 20.

Respiratory and vasomotor center activity during diffusion respiration as shown by action potential discharges in recurrent laryngeal (N) and cervical sympathetic (central end, CS) nerves in cat. Time in seconds. Top: control period. There is a rhythmic discharge in recurrent laryngeal nerve. Each burst of impulses is accompanied by increase in cervical sympathetic discharge. Middle: 1 min after beginning of diffusion respiration. Synchronization of recurrent laryngeal and cervical sympathetic activity is still present. Both discharges are intensified. Bottom: after 16 min of diffusion respiration. Recurrent laryngeal discharge is diminished in intensity and cervical sympathetic discharge no longer shows any rhythmicity.

From Joels and Samueloff 386
Figure 21. Figure 21.

Two tests used to evaluate effects of increased pulmonary afferent activity by lung inflation in decerebrate cat artificially ventilated with respiratory cycle‐triggered pump. A: lung inflation was stopped for 1 respiratory cycle. B: lung inflation started 800 ms (broken line) after onset of expiratory phase; duration of inflation was 750 ms. ITP, intratracheal pressure; PHR, integrated phrenic activity (time constant, 0.1 s); CS, integrated right cervical sympathetic activity (time constant, 0.1 s); SPL, integrated splanchnic activity (time constant, 0.1 s). In A note increased phrenic and sympathetic activity in absence of 1 cycle of lung inflation and in B note decreased sympathetic activity in absence of change in phrenic activity on lung inflation (begun at broken line).

From Gootman et al. 290
Figure 22. Figure 22.

Mechanisms of respiratory sinus arrhythmia: combination of central irradiation or central inspiratory neuronal activity (solid line) and pulmonary reflex (dashed and dotted lines). A: spontaneous activity of inspiratory motoneurons of respiratory center (RC) causes inhibition of cardiac vagal motoneurons (CVMN) and therefore tachycardia. B: tachycardia is enhanced by expansion of lungs, causing further inhibition of cardiac vagal motoneurons (dashed line). C: at height of inspiration, expanded lungs inhibit inspiratory neurons via Hering‐Breuer respiratory reflex and therefore partially restore activity of cardiac vagal motoneurons (dotted line). D: during expiration with lungs in expiratory position, vagal tone is fully restored, leading to bradycardia through combination of cessation of activity of inspiratory neurons and diminution of pulmonary stretch‐receptor activity. +, Stimulation; —, inhibition.

Adapted from Anrep et al. 39
Figure 23. Figure 23.

Effects of withdrawing arterial chemoreceptor drive and of reestablishing lung movements during apneic asphyxia in the dog with systemic circulation is perfused at constant blood flow, separate perfusions of isolated carotid sinuses and isolated aortic arch, closed chest, spontaneous respiration, and no pulmonary circulation. Systemic venous blood is oxygenated in isolated perfused lungs of a donor animal. Carotid sinus, aortic arch, and arterial blood = 133 mmHg, = 45 mmHg, and pH = 7.34. A: at signal, apneic asphyxia is produced by reducing tidal volume of isolated perfused donor lungs from 400 to 75 ml while creating a bilateral open pneumothorax in recipient animal; lungs are held in semi‐inflated position by occluding the trachea. Break in record lasted 3.5 min. B: apneic asphyxia continued (carotid sinus, aortic arch and arterial blood = 74 mmHg, = 70 mmHg, and pH = 7.19). During signal, carotid and aortic body chemoreceptor drive was withdrawn by substituting oxygenated blood ( = 140 mmHg, = 44 mmHg, and pH = 7.39). C: apneic asphyxia continued (carotid sinus, aortic arch and arterial blood = 74 mmHg, = 70 mmHg, and pH = 7.19). During signal, pneumothorax was reduced and spontaneous breathing was temporarily reestablished. D: apneic asphyxia ended at signal. Spontaneous breathing was reestablished and tidal volume of isolated perfused donor lungs was restored to 400 ml. Break in record lasted 4 min. Time calibration, 10 s. HR, heart (atrial) rate; TV, tidal volume (inspiration upward); AAP, aortic arch pressure; CSP, carotid sinus pressure; BP, systemic arterial perfusion blood pressure.

From Angell‐James and Daly 24
Figure 24. Figure 24.

Effects of withdrawal of carotid body (CB) chemoreceptor drive on diving response in seal. Carotid sinus‐CB regions were autoperfused under controlled conditions with arterial blood. Mean values (± SE; n = 11) for respiratory minute volume (), heart rate (HR) and systolic (S), diastolic (D), and mean (M) arterial blood pressure (BP). Filled bars, control values in spontaneously breathing animals before and after experimental dives; stippled bars in second column, values taken 105 s after start of experimental dive; open bars, withdrawal of chemoreceptor drive during dive by perfusion of CBs with blood of high and normal from external oxygenator; stippled bars in fourth column, chemoreceptor drive was reestablished during dive by perfusion of CBs with hypoxic hypercapnic blood from animal's circulation. Values for and for arterial blood (a) and blood perfusing CBs (cb) are expressed in mmHg; pH is expressed in units.

From Daly et al. 181
Figure 25. Figure 25.

Effect of increasing right lung blood flow by average of 133% on average activity of 10 J receptors in right lung. (Blood flow was increased by occluding left pulmonary artery at arrow.) Values are means ± SE.

From Anand and Paintal 17


Figure 1.

Nervous control of respiratory and cardiovascular systems by arterial baroreceptors and chemoreceptors with some other inputs to nervous system by which integration between the 2 systems takes place. and arterial partial pressure of O2 and CO2, respectively.



Figure 2.

Sections of continuous tracing that show effects of changing respiratory rate on relationship between respiration and blood pressure in a human. During breathing, subject followed sinusoidal signal of slowly varying period. Between two slowest (top) and fastest (bottom) respiratory rates there is almost complete reversal of relation of blood pressure change to respiratory phase. Inspiration corresponds to downward movement of spirogram.

From Dornhorest et al. 227 by permission of the American Heart Association, Inc


Figure 3.

Effect of spontaneous respiration on venous return and cardiac output in dog with closed chest. Tracings from top to bottom: time and base line, aortic pressure (mmHg), pulmonary artery pressure, superior vena caval and intrathoracic pressures (mmH2O), pulmonary arterial and superior vena caval flows (ml · min−1). A, beginning of inspiration; S, acceleration of superior vena caval flow during ventricular systole; D, acceleration of superior vena caval flow during ventricular diastole. Stroke volume (ml) is shown below pulmonary arterial flow curve. Volume (ml) through superior vena cava during each cardiac cycle is shown at bottom. Electrical frequency response of both flowmeters is reduced from 400 to 40 Hz. Superior vena caval pressure curve is damped.

From Brecher 87. In: Venous Return, © 1956, Grune & Stratton


Figure 4.

Effects on heart rate and systemic vascular resistance of lung inflation during apneic asphyxia in dog with cardiopulmonary bypass, constant systemic blood flow, closed chest, and spontaneous respiration. Carotid sinus, aortic arch, and arterial blood = 138 mmHg, = 42 mmHg, and pH = 7.35. A: at signal, apneic asphyxia produced by reducing tidal volume of isolated perfused extracorporeal donor lungs from 400 to 75 ml while abolishing recipient's lung movements by injecting 3 mg of decamethonium into systemic arterial inflow tube. Break in record lasted 2 min. B: apneic asphyxia continued (carotid sinus, aortic arch, and arterial blood = 70 mmHg, = 71 mmHg, and pH = 7.19). Two maintained lung inflations with ∼300 ml air injected into trachea. Between B and C: tidal volume of isolated perfused lungs was restored to 400 ml. C: combined stimulation of carotid and aortic bodies by hypoxic hypercapnic blood ( = 40 mmHg, = 51 mmHg, and pH = 7.30). Systemic arterial blood = 130 mmHg, = 41 mmHg, and pH = 7.35. HR, heart (atrial) rate; TV, tidal volume (inspiration upward); AAP, mean aortic arch pressure; CSP, mean carotid sinus pressure; BP, mean systemic arterial perfusion pressure.

From Angell‐James and Daly 24


Figure 5.

Effects of maintained lung inflation with different pressures and volumes on systemic vascular resistance in 3 experiments. A and B: inflation volume and inflation pressure, respectively, are plotted against change in vascular resistance. Between inflations, lungs were allowed to collapse. C and D: same relationships are shown, but lungs were inflated from an expiratory pressure of 4 (○), 6 (•), and 10 (Δ) cmH2O. D: inflation pressure is difference between that at beginning and completion of inflation.

From Daly et al. 186


Figure 6.

A, B, and C: effects of stimulating carotid bodies with hypoxic blood in anesthetized dog on positive‐pressure artificial respiration with open pneumothorax. A and C: control states taken during normal artificial ventilation. Respiratory pump stroke volume = 150 ml, arterial blood = 38 mmHg, and pH = 7.35. B was taken 4 min after increasing stroke volume to 430 ml. Arterial blood = 24 mmHg and pH = 7.49. Frequency of pump was constant at 20 cycles · min−1. CSP, mean carotid sinus perfusion pressure; BP, mean systemic arterial blood pressure; HR, heart rate.

From Daly and Hazzledine 184


Figure 7.

Effects on heart rate of brief carotid body stimuli delivered during different phases of respiratory cycle in spontaneously breathing anesthetized dog. Records of tidal volume (inspiration upward), electrocardiogram (ECG), right atrial pressure (RAP), and arterial blood pressure (BP) are shown. A‐C: injections of CO2‐saline into carotid bifurcation caused brief chemoreceptor stimulation. When these stimuli were delivered during expiration (A and C), they evoked a prompt slowing of the heart and an expiratory effort. When stimuli were delivered during inspiration (B), they evoked an increased inspiratory effort but no change in heart rate. As control, chest was squeezed at D to mimic thoracic and atrial pressure changes seen with chemoreceptor stimuli given in expiration, but this did not affect heart rate.

From Haymet and McCloskey 323


Figure 8.

Modulation by phasic changes in respiration of respiratory and heart‐rate responses to brief stimuli applied to carotid body chemoreceptors by agents injected into common carotid artery. Stimuli were delivered to carotid bodies during inspiratory (○) and expiratory (•) phases of respiratory cycle. Ordinate: phase of respiratory cycle (inspiration, expiration), change in amplitude of inspiration, change in duration of expiration, or change in heart rate. Abscissa: time.

Data from Black and Torrance 81, Eldridge 250, Haymet and McCloskey 323, and M. de B. Daly (unpublished observations)


Figure 9.

Respiratory modulation of cardiac reflex responses to brief stimulations of carotid chemoreceptors and baroreceptors by 2 components, central inspiratory neuronal drive and pulmonary vagal reflex, in anesthetized animal paralyzed with neuromuscular blocking agent. Arrows, timing in relation to respiratory events of brief stimuli applied to carotid bodies (○) or carotid baroreceptors (•). Left: central inspiratory modulation alone; lungs were held in expiratory position to exclude pulmonary reflex component. Right: modulation by lung inflation during cessation of central inspiratory drive. (Compare arrow b with c, and c with d.) Note that lung denervation abolished modulation by lung inflation of chemoreceptor and baroreceptor responses.

Data from Daly and Angell‐James 178, Davidson et al. 203, and Gandevia et al. 273


Figure 10.

Effects of elective sustained stimulation of isolated perfused carotid body chemoreceptors by hypoxic hypercapnic blood on heart rate and respiration in spontaneously breathing animals. Relationship between changes in heart rate and respiratory minute volume under steady‐state conditions. •, Dog 193; ○, cat 191,486; x, seal 252; Δ, monkey 187.



Figure 11.

Reflex effects of lung inflation on vasoconstrictor responses elicited by stimulation of carotid bodies (CB) and aortic bodies (AB) in dog with cardiopulmonary bypass, constant systemic blood flow, open pneumothorax, and no ventilation of lungs. Separate perfusions of isolated carotid sinuses and of isolated aortic arch with blood from disk equilibrator ( = 140 mmHg, = 47 mmHg, and pH = 7.34). A‐D, effects of stimulation of CB and AB by hypoxic hypercapnic blood ( = 21 mmHg, = 83 mmHg and pH = 7.17) during continuous signal. Between arrows, lungs were inflated with 300 ml of room air. Between B and C, lungs were denervated. Note abolition of effects of lung inflation in C and D. At X, paper was stopped for 1.5 min. CSP, mean carotid sinus pressure; AAP, mean aortic arch pressure; BP, mean systemic arterial blood pressure. Time marker, 10 s.



Figure 12.

Central respiratory modulation of heart rate (HR) during stimulation of carotid body chemoreceptors in anesthetized dog with open chest and positive‐pressure ventilation. Both lungs are denervated by method of Daly and Scott 193. Av ENG, averaged phrenic electroneurogram; ENG, phrenic electroneurogram (efferent activity); ITP, intratracheal pressure; RM, rib movements (inspiration upward); BP, arterial blood pressure (mean and phasic). At signal, there was an intracarotid injection of 5 μg · kg−1 of sodium cyanide. Time marker, 10 s.

From Daly and Angell‐James 178


Figure 13.

Effects on changes in P‐P (P‐wave) interval of stimulating carotid baroreceptors (neck suction, −30 mmHg) for 0.6 s during early inspiration (left) and during expiration (right). Averaged P‐P intervals for 6 normal human subjects. •, Spontaneous changes provoked by inspiration without baroreceptor stimulation (0 mmHg); ▴, changes in pulse interval after neck suction applied in early inspiration; ▪, net response to baroreceptor stimulation (difference) calculated by subtracting responses without neck suction from responses with neck suction. TV, tidal volume

From Eckbere and Orshan 246


Figure 14.

Effects in 1 subject of single breath on cardiac response produced by stimulation of carotid sinus baroreceptors during period of apnea in expiratory position started 5 s earlier. Top: during apnea, 3 tests of baroreceptor stimulation started at zero time. In 2 tests (○, ▴), a single breath was taken, ↑, Start of inspiration; ↓, peak of inspiration and beginning of expiration. Bottom: 2 tests of apnea started at zero time. In one test (□), a single breath was superimposed as indicated by arrows. (J. E. Angell‐James and M. de B. Daly, unpublished observations.)



Figure 15.

Reflex interactions between inputs from trigeminal facial receptors (stimulated by water during experimental dive) and carotid body chemoreceptors. Effects of stimulating carotid body chemoreceptors alone [▪; (CB)] and during experimental dives [▪; (ED + CB)] on pulse interval and respiratory minute volume; experimental dives alone [□; (ED)]; control values [•; (C)]. Values are means ± SE from 10 tests in 5 animals. Where SE bars are not given, SE is less than size of symbol.

From Eisner et al. 252


Figure 16.

Effects of stimulating carotid body chemoreceptors with cyanide (7.0 μg · kg−1) alone and during period of apnea reflexly induced by electrical stimulation of central end of a superior laryngeal nerve in dog with intermittent positive‐pressure ventilation and open pneumothorax. A: superior laryngeal nerve stimulation (3V, 1 ms, 15 Hz). B: carotid body (CB) stimulation alone. C: carotid body stimulation during stimulation of superior laryngeal nerve. Repeat stimulation of carotid body alone (not shown) had effect similar to that shown in B. ITP, intratracheal pressure; RM, movements of the ribs (inspiration upward); BP, arterial blood pressure. Time calibration and time marker, 10 s.

From Angell‐James and Daly 31


Figure 17.

Three‐dimensional plot of relationship between time (t), pulse interval (PI) and volume (Vt) of right (test) lung (filled areas) during electrical stimulation of superior laryngeal nerve with stimulation of carotid body chemoreceptors by intracarotid cyanide in anesthetized dog with open pneumothorax. Tracheal divider separated left and right lung airways. Artificial ventilation of naturally perfused denervated left lung. Right lung was innervated, but pulmonary artery blood flow was obstructed by balloon. A: electrical stimulation of superior laryngeal nerve (bar) combined with intracarotid injection of cyanide at beginning of bar while right lung was in expiratory position (zero volume). B: right lung in expiratory position during combined stimulation of a superior laryngeal nerve and carotid body (bar) followed by inflation of right lung at arrow. Between B and C, right lung was denervated. C: inflation of right lung began at arrow during combined stimulation of superior laryngeal nerve and carotid body.

From Angell‐James and Daly 32


Figure 18.

Effects of stimulating carotid body chemoreceptors on carotid sinus baroreceptor control of muscle vascular resistance in 9 anesthetized, artificially ventilated, paralyzed, and vagotomized cats. Graphs show relationship between pressure in partly isolated perfused carotid sinuses and muscle vascular resistance (A) and arterial blood pressure (B). •—•, No carotid body stimulation; ○—○, with carotid body stimulation. C: carotid sinus pressure is related to the differences between the responses in A and B in terms of muscle vascular resistance (○) and arterial blood pressure (□), respectively, obtained at each carotid sinus pressure level with and without coexisting chemoreceptor stimulation. Values are means ± SE of numerous tests.

From Wennergren et al. 663


Figure 19.

Interactions between carotid baroreceptors and chemoreceptors in cat anesthetized with Althesin. A: response produced by inflating carotid blind sac to 210 mmHg. B: response evoked by stimulating carotid chemoreceptors with saline equilibrated with CO2 C: effect of stimulating chemoreceptors during an ongoing baroreceptor reflex. Resp., respiratory air flow; Vm, respiratory minute volume; HR, heart rate; BP, arterial blood pressure. In C, baroreceptor reflex was fully suppressed on chemoreceptor stimulation.

From Marshall 499


Figure 20.

Respiratory and vasomotor center activity during diffusion respiration as shown by action potential discharges in recurrent laryngeal (N) and cervical sympathetic (central end, CS) nerves in cat. Time in seconds. Top: control period. There is a rhythmic discharge in recurrent laryngeal nerve. Each burst of impulses is accompanied by increase in cervical sympathetic discharge. Middle: 1 min after beginning of diffusion respiration. Synchronization of recurrent laryngeal and cervical sympathetic activity is still present. Both discharges are intensified. Bottom: after 16 min of diffusion respiration. Recurrent laryngeal discharge is diminished in intensity and cervical sympathetic discharge no longer shows any rhythmicity.

From Joels and Samueloff 386


Figure 21.

Two tests used to evaluate effects of increased pulmonary afferent activity by lung inflation in decerebrate cat artificially ventilated with respiratory cycle‐triggered pump. A: lung inflation was stopped for 1 respiratory cycle. B: lung inflation started 800 ms (broken line) after onset of expiratory phase; duration of inflation was 750 ms. ITP, intratracheal pressure; PHR, integrated phrenic activity (time constant, 0.1 s); CS, integrated right cervical sympathetic activity (time constant, 0.1 s); SPL, integrated splanchnic activity (time constant, 0.1 s). In A note increased phrenic and sympathetic activity in absence of 1 cycle of lung inflation and in B note decreased sympathetic activity in absence of change in phrenic activity on lung inflation (begun at broken line).

From Gootman et al. 290


Figure 22.

Mechanisms of respiratory sinus arrhythmia: combination of central irradiation or central inspiratory neuronal activity (solid line) and pulmonary reflex (dashed and dotted lines). A: spontaneous activity of inspiratory motoneurons of respiratory center (RC) causes inhibition of cardiac vagal motoneurons (CVMN) and therefore tachycardia. B: tachycardia is enhanced by expansion of lungs, causing further inhibition of cardiac vagal motoneurons (dashed line). C: at height of inspiration, expanded lungs inhibit inspiratory neurons via Hering‐Breuer respiratory reflex and therefore partially restore activity of cardiac vagal motoneurons (dotted line). D: during expiration with lungs in expiratory position, vagal tone is fully restored, leading to bradycardia through combination of cessation of activity of inspiratory neurons and diminution of pulmonary stretch‐receptor activity. +, Stimulation; —, inhibition.

Adapted from Anrep et al. 39


Figure 23.

Effects of withdrawing arterial chemoreceptor drive and of reestablishing lung movements during apneic asphyxia in the dog with systemic circulation is perfused at constant blood flow, separate perfusions of isolated carotid sinuses and isolated aortic arch, closed chest, spontaneous respiration, and no pulmonary circulation. Systemic venous blood is oxygenated in isolated perfused lungs of a donor animal. Carotid sinus, aortic arch, and arterial blood = 133 mmHg, = 45 mmHg, and pH = 7.34. A: at signal, apneic asphyxia is produced by reducing tidal volume of isolated perfused donor lungs from 400 to 75 ml while creating a bilateral open pneumothorax in recipient animal; lungs are held in semi‐inflated position by occluding the trachea. Break in record lasted 3.5 min. B: apneic asphyxia continued (carotid sinus, aortic arch and arterial blood = 74 mmHg, = 70 mmHg, and pH = 7.19). During signal, carotid and aortic body chemoreceptor drive was withdrawn by substituting oxygenated blood ( = 140 mmHg, = 44 mmHg, and pH = 7.39). C: apneic asphyxia continued (carotid sinus, aortic arch and arterial blood = 74 mmHg, = 70 mmHg, and pH = 7.19). During signal, pneumothorax was reduced and spontaneous breathing was temporarily reestablished. D: apneic asphyxia ended at signal. Spontaneous breathing was reestablished and tidal volume of isolated perfused donor lungs was restored to 400 ml. Break in record lasted 4 min. Time calibration, 10 s. HR, heart (atrial) rate; TV, tidal volume (inspiration upward); AAP, aortic arch pressure; CSP, carotid sinus pressure; BP, systemic arterial perfusion blood pressure.

From Angell‐James and Daly 24


Figure 24.

Effects of withdrawal of carotid body (CB) chemoreceptor drive on diving response in seal. Carotid sinus‐CB regions were autoperfused under controlled conditions with arterial blood. Mean values (± SE; n = 11) for respiratory minute volume (), heart rate (HR) and systolic (S), diastolic (D), and mean (M) arterial blood pressure (BP). Filled bars, control values in spontaneously breathing animals before and after experimental dives; stippled bars in second column, values taken 105 s after start of experimental dive; open bars, withdrawal of chemoreceptor drive during dive by perfusion of CBs with blood of high and normal from external oxygenator; stippled bars in fourth column, chemoreceptor drive was reestablished during dive by perfusion of CBs with hypoxic hypercapnic blood from animal's circulation. Values for and for arterial blood (a) and blood perfusing CBs (cb) are expressed in mmHg; pH is expressed in units.

From Daly et al. 181


Figure 25.

Effect of increasing right lung blood flow by average of 133% on average activity of 10 J receptors in right lung. (Blood flow was increased by occluding left pulmonary artery at arrow.) Values are means ± SE.

From Anand and Paintal 17
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Article Title: Interactions Between Respiration and Circulation
 

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M. De Burgh Daly. Interactions Between Respiration and Circulation. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 529-594. First published in print 1986. doi: 10.1002/cphy.cp030216