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Interaction of Cardiovascular Reflexes in Circulatory Control

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Abstract

The sections in this article are:

1 Determinants of Neurogenic Control
2 Definitions
2.1 Cardiovascular Reflex Arc
2.2 Open‐Loop Versus Closed‐Loop Response
2.3 Types of Interactions
3 Central Nervous System Substrate
3.1 Medullary Nuclei
3.2 Hypothalamus and Cardiovascular Control
3.3 Inferior Olive: Suppression of Baroreflex
3.4 Cerebellar Control: Hypothalamic and Baroreceptor Interactions
3.5 Suprabulbar and Cortical Connections
3.6 Sleep and Sinoaortic Reflexes
3.7 Respiratory Influences on Baroreceptor Control of Vagal Neurons
3.8 Spinal Preganglionic Sympathetic Neurons
3.9 Medullary Preganglionic Vagal Neurons to Heart
3.10 Neuropeptides: Regulation of Arterial Pressure
3.11 Brain Amines: Reflex Control
4 Cardiovascular Reflexes that Might Interact
4.1 Sinoaortic Baroreflexes
4.2 Cardiac Receptors With Afferent Vagal Fibers
4.3 Cardiac Receptors With Afferent Sympathetic Fibers
4.4 Reflexes Originating From Chemoreceptor Stimulation
4.5 Reflexes Originating in Lung
4.6 Reflexes Originating In Skeletal Muscle During Exercise
4.7 Reflexes Originating From Facial and Upper Airway Receptors: Diving Reflex
4.8 Vestibulocerebellar Reflexes
5 Interaction of Specific Reflexes in Autonomic Control of Circulation
5.1 Selectivity and Nonuniformity of Autonomic Control When One Sensory Afferent Input is Activated or Withdrawn
5.2 Simultaneously Activating Sensory Stimuli
5.3 Redundancy in Baroreceptor Control of Preganglionic Neurons
5.4 Sensitizing Sensory Receptors and Modulating Efferent Sympathetic Neurotransmission
5.5 Regulating Renin and Vasopressin
6 Clinical Implications
6.1 Integrated Neural Responses to Myocardial Ischemia and Infarction
6.2 Interaction of Reflexes in Heart Failure
6.3 Reflex Interactions in Hypertension
7 Conclusion
Figure 1. Figure 1.

Schematic of open‐loop vs. closed‐loop reflex responses. In latter condition, response modifies sensory input caused by a specific stimulus.

Figure 2. Figure 2.

Three examples of summation and interaction of reflexes causing directionally similar responses. Hypothetical patterns of afferent convergence are diagrammed with anticipated responses. Carotid sinus nerves and aortic nerves inhibit sympathetic neurons and activate vagal neurons. Apnea and facial immersion activate vagal neurons. Sympathetic neurons but not vagal neurons seem to show redundancy (see also Fig. ).

Figure 3. Figure 3.

Summation and interaction of reflexes causing opposite responses. Hypothetical pre‐ and postsynaptic interactions explain observed responses. Solid lines, inhibition of sympathetic efferent activity caused by activating arterial baroreceptors (A, B, C) or electrically stimulating cardiac vagal afferents (D). Dashed lines, influence of simultaneous stimulation of chemoreceptors. A: no change in any parameter except for simple additive shift of the baroreceptor curve upward with chemoreceptor stimulation; B: increased baroreflex threshold, but chemoreceptor stimulation changes neither gain nor range. C: increased threshold and baroreflex gain and inhibited chemoreflex at high arterial pressure. This interaction more closely represents interaction between chemoreceptors and baroreceptors with respect to renal and muscle resistances . D: cardiac reflex inhibited by stimulation of chemoreceptors with respect to muscle resistance .

Figure 4. Figure 4.

A: relationship between carotid baroreceptor stimulation and gracilis perfusion pressure without and with stimulating carotid chemoreceptors in dog. Baroreflex gain is increased and the chemoreflex is suppressed at high carotid sinus pressure. B : interaction between arterial baroreceptors and chemoreceptors (systemic hypoxia) with respect to renal and splanchnic nerve activity in rabbit. Interaction with respect to the renal nerve activity is similar to that in Fig. C.

A from Heistad, Abboud, et al. by copyright permission of the American Society for Clinical Investigation; B from Korner
Figure 5. Figure 5.

Influence of changes in carotid transmural pressure on reflex changes in arterial pressure in normotensive (N) and hypertensive (H) subjects. Curve H shifts to right, and the set point (arrow) is closer to threshold transmural pressure than on curve N, which may account for reported differences in responses to carotid distension and compression in H vs. N subjects.

Adapted from Mancia et al.
Figure 6. Figure 6.

Changes in hindlimb perfusion pressure (mean ± SE) with changes in frequency of stimulation of lumbar sympathetic nerves in rabbits. Stimulation varied around a low base‐line frequency averaging 1.5 Hz (curve A) and a high base‐line frequency averaging 4 Hz (curve B). Slope of resistance change for a similar change in frequency of stimulation was the same or less in curve B than in curve A.

From Guo, Thames, and Abboud , by permission of the American Heart Association
Figure 7. Figure 7.

Comparison of reflex increases in gracilis muscle perfusion pressure (mean ± SE) during stimulation of somatic afferents (left panel) and intra‐arterial norepinephrine (right panel) at levels of carotid sinus pressure (75, 125, and 175 mmHg). Decreased reactivity to norepinephrine did not suppress somatic reflex at high carotid sinus pressure.

From Abboud, Mark, and Thames , by permission of the American Heart Association
Figure 8. Figure 8.

Distribution of major excitatory and inhibitory nuclei and pathways in medulla (A, B, C), suprabulbar regions (A), and spinal cord (D). A: bulbar and suprabulbar regions. Solid lines, ascending pathways to reticulobulbar formation and then to hypothalamus (Hypoth), septum (S), amygdala (Am), and neocortex; to the thalamus, limbic system, and neocortex; and to cerebellum. Descending pathways (dashed lines) may originate in neocortex, limbic system, hypothalamus, or cerebellum [fastigial nucleus (FN)]. LC, locus ceruleus; ON, olivary nucleus; TS, tractus solitarius; IX and X, carotid sinus and vagal afferents, respectively. B: dorsal surface of medulla. Nucleus tractus solitarius (NTS) and TS projected onto dorsal surface of medulla and floor of 4th ventricle. Carotid sinus nerve afferents, carotid baroreceptors, and glossopharyngeal nerve (dashed area) and aortic nerve afferents and vagus nerve (dotted area) centrally projected. C: transverse section of medulla near obex. Note major cardiovascular nu‐ B clei and areas of noradrenergic and serotonergic (B2) neurons. Neurons containing catecholamines, dopamine, or serotonin are distributed in groups throughout central nervous system (CNS). A1 and A2, medullary noradrenergic groups connected to bulbospinal tracts that regulate cardiovascular function. A1 group is inhibitory. A2 neurons innervate NTS; their destruction causes hypertension. Locus ceruleus, another major catecholaminergic group of neurons is more rostral in dorsomedial medulla. B1 neurons are predominantly in and around raphe nuclei (R) in medulla and midbrain. Serotonergic bulbospinal tract may regulate preganglionic sympathetic neurons or inhibitory interneurons. AP, area postrema; XII, hypoglossal nucleus; X, dorsal motor nucleus of vagus; C and EC, cuneate and external cuneate; NA, nucleus ambiguus; SNV, spinal nucleus of trigeminal; LRN, lateral reticular nucleus; 10, inferior olivary nucleus; PMR, paramedial reticular nucleus. D: transverse section of thoracic spinal cord shows excitatory descending pathway (E) distribution from LRN and inhibitory descending pathways (I) from R, PMR, and ventromedial medulla. Preganglionic sympathetic neurons in intermediolateral horn (IML) are excitatory. Interneurons that may modulate IML activity have been described. Gebber and McCall in 1976 described excitatory interneurons near preganglionic neurons that are not activated antidromically but by stimulating medullary pressor sites ∼10 ms earlier than antidromically driven preganglionic neurons. McCall et al. in 1977 described neurons in intermediomedial region (IMM) of spinal gray that inhibit preganglionic excitatory neurons (believed to be inhibitory interneurons).

A and D adapted from Korner ; B adapted from Spyer ; C adapted from Loewy et al.
Figure 9. Figure 9.

Excitatory and inhibitory pathways regulating medullary pressor and depressor areas and preganglionic spinal sympathetic neurons (IML, IMM) and preganglionic medullary vagal neurons (VN). VRN, ventral reticular nuclei; A1, inhibitory noradrenergic neurons in ventral part of LRN; NE, norepinephrine; Ach, acetylcholine; Ms, skeletal muscle; Art. Baro., arterial baroreflex. Solid lines, pathways that stimulate neurons; dotted lines, pathways that suppress neurons.

Figure 10. Figure 10.

Activation of vagal neurons by anterior hypothalamus (Ant. Hypoth.) and NTS causing bradycardia (left) and inhibition of vagal neurons by the posterior hypothalamus (Post. Hypoth.) and by respiratory neurons causing tachycardia (right). V, respiratory neuronal activity that inhibits vagal neurons causing tachycardia; atropine blocks this inhibition.

Figure 11. Figure 11.

Electrical stimulation of diencephalon in decorticate paralyzed cats triggers simultaneously central hyperventilation (increased phrenic nerve activity) and increased motor activity of both biceps femoris nerves. Hyperventilation clearly does not depend on peripheral stimulus from contracting muscle or chemoreceptors.

From Eldridge et al.
Figure 12. Figure 12.

Cardiovascular responses to desynchronized sleep (means ± SE) before (solid lines) and after (dashed lines) sinoaortic denervation (6 episodes; 1 cat). Sleep induces hypotension, mesenteric vasodilatation, and iliac vasodilatation, but latter is reflexly buffered and reversed to vasoconstriction when baroreflexes are intact (solid lines). Sinoaortic denervation unmasks dilatation.

From Baccelli et al. , by permission of the American Heart Association
Figure 13. Figure 13.

A: carotid sinus blood pressure (BP), air flow, and single cardiac vagal efferent nerve (CVE) activity in dogs. Burst of firing caused by baroreceptor stimulation occurs only in expiration. B: effect of repeated brief baroreceptor stimulations by neck suction in humans (lower tracing) on RR interval (HP), during expiration (suctions 1, 3), and during inspiration (suctions 2, 4). Reflex bradycardia is greater during expiration.

A from Spyer ; B adapted from Trzebski et al.
Figure 14. Figure 14.

Excitatory neurons of vasomotor center (VMC) in brain stem [catecholaminergic (CA) or serotonergic (5‐HT)] may stimulate preganglionic neurons in IML to increase sympathetic activity and cause hypertension. Normally inhibited, these neurons are disinhibited by 1) decreased activity of inhibitory central CA nerves to VMC as in DOCA‐salt or renal hypertension, 2) decreased activity of arterial baroreceptor nerve or other central CA nerves to NTS, or 3) decreased activity of inhibitory CA nerves between NTS and VMC.

From Chalmers , by permission of the American Heart Association
Figure 15. Figure 15.

Stimulation of the carotid chemoreceptors with nicotine causes a reflex fall in coronary perfusion pressure (PP) and coronary vasodilatation during constant cardiac pacing and constant coronary blood flow (perfusion pump). Dilatation is not metabolic in view of the rise in coronary sinus O2 pressure (PO2). Atropine and vagotomy partially block it.

From Heistad and Abboud , by permission of the American Heart Association
Figure 16. Figure 16.

Activating carotid chemoreceptors by carotid hypoxemia causes hypertension, bradycardia, and reflex vasodilatation in paw and constriction in muscle. Paw and muscle perfused separately at constant blood flow. Carotid baroreceptor stimulation (BARO) in contrast causes hypotension, bradycardia, and vasodilatation in muscle and paw. SAP, systemic arterial pressure.

From Abboud et al. and Heistad, Abboud, et al.
Figure 17. Figure 17.

Dopamine (1 and 5 μg/kg−‐1/min) suppresses hyperventilatory response ( ) to hypoxia (10% O2) in humans. Minimal suppression during normoxia; none during hyperoxia, suggesting chemoreceptor mediation of dopamine action.

From Heistad and Abboud , by permission of the American Heart Association
Figure 18. Figure 18.

Blood flow to gracilis muscle (Grac. M.) and paw maintained constant with pump. During sustained stimulation of carotid sinus nerve (CSS), close to bulb to exclusively activate baroreceptor nerves, withdrawal of sympathetic tone caused reflex hypotension and dilatation in muscle and paw. Cyanide (CN) injected into ascending aorta during electrical stimulation of baroreceptors activated chemoreceptors, causing vasoconstriction in muscle and further dilatation in paw.

From Calvelo, Abboud, et al. , by permission of the American Heart Association
Figure 19. Figure 19.

Repeated brief (2‐min) carotid sinus nerve (CSN) stimulations (25 Hz, 0.5 ms, 0.25‐1.5 V; heavy horizontal lines), resulting in significant increases in phrenic nerve activity that outlast stimulus by up to 5 min of afterdischarge. Also inspiratory activity has long‐lasting increase (> 30 min) that becomes progressively larger with each stimulus and is blocked by intravenous methysergide (lower panel). Data normalized so highest value during stimulation equals 100 units. Partial CO2 pressure is 34 mmHg.

From Millhorn et al.
Figure 20. Figure 20.

Pressor responses to ischemic exercise in normal leg (solid line) and insensitive leg (dashed line) were similar. Ischemia of normal leg without exercise sustained pressor response, but ischemia of insensitive leg did not.

From Rowell et al. , by permission of the American Heart Association, adapted from Alam and Smirk
Figure 21. Figure 21.

Electrical lumbar nerve stimulation (0.1‐100 Hz) causes significant constriction in arterioles of gracilis muscle (solid lines) and hind paw (dashed lines) of dog, as indicated by marked increases in perfusion pressures at constant blood flow. Constriction is much more pronounced in venules and veins of paw than in muscle. In contrast to responses to direct nerve stimulation, reflex vasoconstrictor responses to chemoreceptor stimulation are selective to arterioles in muscle (Figs. , ). cps, Cycles per second.

From Calvelo, Abboud, et al. , by permission of the American Heart Association
Figure 22. Figure 22.

Changes in heart rate (HR) and renal and muscle resistances during stimulation of cardiac afferents (upper panels) and arterial baroreceptors (lower panels). Both sets of afferents are inhibitory with some selectivity. For example, cardiac afferents cause a significantly greater inhibition of renal resistance. Interactions between arterial baroreceptors and cardiac afferents and input from chemoreceptors and hypothalamic defense area cause a variety of responses. Variable interactions point to specificity in patterns of afferent convergence on various groups of brain stem neurons or connecting pathways. For example, chemoreceptor stimulation prevents cardiac afferents from inhibiting skeletal muscle resistance but does not influence inhibitory influence of arterial baroreceptors. (Schematic drawn from data in refs. ).

Figure 23. Figure 23.

Reduced forearm blood flow (Plethysmographic tracings in upper panels) and forearm volume at constant venous congesting pressure of 20 mmHg (lower panels) indicate increases in arteriolar resistances and venous tone, respectively. Responses are to intra‐arterial infusions of norepinephrine (left panels) and to lower‐body negative pressure (LBNP, −60 mmHg) sufficient to lower arterial pressure and pulse pressure (right panels). Arteriolar constriction was comparable with 2 interventions, but venous tone increase was negligible during LBNP compared to intra‐arterial NE.

From Abboud et al.
Figure 24. Figure 24.

Upnght tilt does not increase venous tone in calf of humans. Veins of limbs are not sensitive to arterial or cardiopulmonary baroreflexes, but arterioles are. Other venous segments, e.g., splanchnic veins, are sensitive to these baroreflexes, whereas veins of extremities are more sensitive to temperature or respiratory reflexes (cf. Fig. ).

From Abboud et al.
Figure 25. Figure 25.

Hyperventilatory response to stimulating carotid chemoreceptors with nicotine is augmented during systemic hypotension and inhibited during hypertension in anesthetized dogs. The rise in systemic arterial pressure suppresses base‐line ventilation, which tends to increase during hypotension.

From Heistad, Abboud, et al.
Figure 26. Figure 26.

Responses (means ± SE) to electrical stimulation of somatic afferents during volume expansion and after bilateral vagotomy (V). Volume expansion with +5, +10, and +15 ml/kg of 6% dextran in normal saline suppressed reflex renal vasoconstrictor response to electrical stimulation of somatic afferents in dogs with sinoaortic deafferentation as compared to control (C). Bilateral vagotomy markedly increased reflex vasoconstriction. Neither volume expansion nor vagotomy altered reflex increases in arterial pressure or heart rate.

From Thames and Abboud
Figure 27. Figure 27.

Effect of sequential denervation of carotid sinus nerves (C), aortic afferents (A), and vagi (V) in anesthetized rabbits. Means ± SE of increases in arterial pressure, perfusion pressure in the hindlimb (perfused at constant blood flow), and heart rate are shown. Denervation of carotid sinus nerves when aortic afferents are intact or after vagotomy causes much smaller increases in arterial pressure and perfusion pressure than their denervation after aortic afferents are cut. The same is true for aortic nerves before and after section of carotid sinus nerves and vagotomy. Also bilateral vagotomy causes much smaller increases in pressures when carotid and aortic afferents are intact than when they have been cut. These interactions are not apparent with respect to heart rate.

Figure 28. Figure 28.

Reflex changes in heart rate (upper panels) and in hindlimb perfusion pressure (lower panels) in anesthetized rabbits during changes in arterial pressure provoked with phenylephrine (PE) and nitroglycerin (NG). Solid lines, control responses; dashed lines, responses after section of carotid sinus nerves (CBRX; A panels) or aortic nerves (ABRX; B panels), or after sinoaortic denervation (SAD; C panels). Sectioning 1 set of afferents significantly reduces gain of baroreflex control of heart rate but not of hindlimb vascular resistance.

From Guo, Thames, and Abboud , by permission of the American Heart Association
Figure 29. Figure 29.

Left: effect of volume expansion with intravenous dextran in an anesthetized dog; integrated renal nerve activity declines. Right: correlations between changes in renal nerve activity (ΔRNA) and mean arterial pressure (ΔMAP) or mean pulmonary artery wedge pressure (PAW) during volume expansion. Sinoaortic denervation (SAD) had a minimal effect on changes in renal nerve activity, whereas bilateral vagotomy essentially abolished reflex.

From Abboud and Thames, Miller, and Abboud
Figure 30. Figure 30.

Left carotid sinus nerve activity decreases despite constant distending volume and isolated left carotid sinus pressure. Decrease resulted from a reflex triggered by distending right carotid sinus, causing withdrawal of sympathetic drive.

From Felder, Heesch, and Thames
Figure 31. Figure 31.

Responses (mean ± SE) of carotid sinus nerve activity during changes in carotid sinus pressure (Cvp, CN) before and after exposure of the carotid sinus to verapamil (VP; 5 μg/ml) or nifedipine (N; 10 μg/ml). *P < 0.05 for difference in slope of responses. (VP, 5 dogs; N, 6 dogs.)

From Heesch, Thames, and Abboud
Figure 32. Figure 32.

Activity of atrial vagal afferents during volume expansion in control dogs (solid line) and dogs in heart failure (dashed lines) in correlation to central venous pressure and left atrial pressure . The afferent activity is markedly impaired in heart failure.

Adapted from Greenberg et al , by permission of the American Heart Association, and Zucker et al.
Figure 33. Figure 33.

Interaction between somatic afferents and arterial and cardiopulmonary afferents. Reflex vasoconstrictor response to activating somatic afferents is augmented when inhibitory input for arterial and cardiopulmonary receptors is impaired.

From Abboud, Thames, and Mark
Figure 34. Figure 34.

Ouabain enhances atrial receptor discharge during volume expansion for similar levels of left atrial pressure (LAP) . Acetylstrophanthidin (AS) in coronary arteries enhances reflex inhibition of renal efferent nerve activity in anesthetized dogs for equivalent level of LAP. No inhibition is seen after bilateral vagotomy.

Adapted from Thames, Waickman, and Abboud and Zucker et al.
Figure 35. Figure 35.

Left panel: interaction between activity of cardiac vagal afferents and carotid baroreflex control of renal nerve activity in anesthetized dogs. Reduction in carotid sinus pressure in dogs with section of the aortic depressor nerves causes significant increases in renal nerve activity Reflex gain in bar graphs (means ± SE of renal nerve activity change in Hz per unit change in arterial pressure) declines significantly during occlusion of circumflex (Cx) but not during occlusion of left anterior descending arteries (LAD). After bilateral vagotomy, gain is markedly enhanced and Cx and LAD occlusion have no effect on the gain.

Data from Abboud and Waickman and Abboud


Figure 1.

Schematic of open‐loop vs. closed‐loop reflex responses. In latter condition, response modifies sensory input caused by a specific stimulus.



Figure 2.

Three examples of summation and interaction of reflexes causing directionally similar responses. Hypothetical patterns of afferent convergence are diagrammed with anticipated responses. Carotid sinus nerves and aortic nerves inhibit sympathetic neurons and activate vagal neurons. Apnea and facial immersion activate vagal neurons. Sympathetic neurons but not vagal neurons seem to show redundancy (see also Fig. ).



Figure 3.

Summation and interaction of reflexes causing opposite responses. Hypothetical pre‐ and postsynaptic interactions explain observed responses. Solid lines, inhibition of sympathetic efferent activity caused by activating arterial baroreceptors (A, B, C) or electrically stimulating cardiac vagal afferents (D). Dashed lines, influence of simultaneous stimulation of chemoreceptors. A: no change in any parameter except for simple additive shift of the baroreceptor curve upward with chemoreceptor stimulation; B: increased baroreflex threshold, but chemoreceptor stimulation changes neither gain nor range. C: increased threshold and baroreflex gain and inhibited chemoreflex at high arterial pressure. This interaction more closely represents interaction between chemoreceptors and baroreceptors with respect to renal and muscle resistances . D: cardiac reflex inhibited by stimulation of chemoreceptors with respect to muscle resistance .



Figure 4.

A: relationship between carotid baroreceptor stimulation and gracilis perfusion pressure without and with stimulating carotid chemoreceptors in dog. Baroreflex gain is increased and the chemoreflex is suppressed at high carotid sinus pressure. B : interaction between arterial baroreceptors and chemoreceptors (systemic hypoxia) with respect to renal and splanchnic nerve activity in rabbit. Interaction with respect to the renal nerve activity is similar to that in Fig. C.

A from Heistad, Abboud, et al. by copyright permission of the American Society for Clinical Investigation; B from Korner


Figure 5.

Influence of changes in carotid transmural pressure on reflex changes in arterial pressure in normotensive (N) and hypertensive (H) subjects. Curve H shifts to right, and the set point (arrow) is closer to threshold transmural pressure than on curve N, which may account for reported differences in responses to carotid distension and compression in H vs. N subjects.

Adapted from Mancia et al.


Figure 6.

Changes in hindlimb perfusion pressure (mean ± SE) with changes in frequency of stimulation of lumbar sympathetic nerves in rabbits. Stimulation varied around a low base‐line frequency averaging 1.5 Hz (curve A) and a high base‐line frequency averaging 4 Hz (curve B). Slope of resistance change for a similar change in frequency of stimulation was the same or less in curve B than in curve A.

From Guo, Thames, and Abboud , by permission of the American Heart Association


Figure 7.

Comparison of reflex increases in gracilis muscle perfusion pressure (mean ± SE) during stimulation of somatic afferents (left panel) and intra‐arterial norepinephrine (right panel) at levels of carotid sinus pressure (75, 125, and 175 mmHg). Decreased reactivity to norepinephrine did not suppress somatic reflex at high carotid sinus pressure.

From Abboud, Mark, and Thames , by permission of the American Heart Association


Figure 8.

Distribution of major excitatory and inhibitory nuclei and pathways in medulla (A, B, C), suprabulbar regions (A), and spinal cord (D). A: bulbar and suprabulbar regions. Solid lines, ascending pathways to reticulobulbar formation and then to hypothalamus (Hypoth), septum (S), amygdala (Am), and neocortex; to the thalamus, limbic system, and neocortex; and to cerebellum. Descending pathways (dashed lines) may originate in neocortex, limbic system, hypothalamus, or cerebellum [fastigial nucleus (FN)]. LC, locus ceruleus; ON, olivary nucleus; TS, tractus solitarius; IX and X, carotid sinus and vagal afferents, respectively. B: dorsal surface of medulla. Nucleus tractus solitarius (NTS) and TS projected onto dorsal surface of medulla and floor of 4th ventricle. Carotid sinus nerve afferents, carotid baroreceptors, and glossopharyngeal nerve (dashed area) and aortic nerve afferents and vagus nerve (dotted area) centrally projected. C: transverse section of medulla near obex. Note major cardiovascular nu‐ B clei and areas of noradrenergic and serotonergic (B2) neurons. Neurons containing catecholamines, dopamine, or serotonin are distributed in groups throughout central nervous system (CNS). A1 and A2, medullary noradrenergic groups connected to bulbospinal tracts that regulate cardiovascular function. A1 group is inhibitory. A2 neurons innervate NTS; their destruction causes hypertension. Locus ceruleus, another major catecholaminergic group of neurons is more rostral in dorsomedial medulla. B1 neurons are predominantly in and around raphe nuclei (R) in medulla and midbrain. Serotonergic bulbospinal tract may regulate preganglionic sympathetic neurons or inhibitory interneurons. AP, area postrema; XII, hypoglossal nucleus; X, dorsal motor nucleus of vagus; C and EC, cuneate and external cuneate; NA, nucleus ambiguus; SNV, spinal nucleus of trigeminal; LRN, lateral reticular nucleus; 10, inferior olivary nucleus; PMR, paramedial reticular nucleus. D: transverse section of thoracic spinal cord shows excitatory descending pathway (E) distribution from LRN and inhibitory descending pathways (I) from R, PMR, and ventromedial medulla. Preganglionic sympathetic neurons in intermediolateral horn (IML) are excitatory. Interneurons that may modulate IML activity have been described. Gebber and McCall in 1976 described excitatory interneurons near preganglionic neurons that are not activated antidromically but by stimulating medullary pressor sites ∼10 ms earlier than antidromically driven preganglionic neurons. McCall et al. in 1977 described neurons in intermediomedial region (IMM) of spinal gray that inhibit preganglionic excitatory neurons (believed to be inhibitory interneurons).

A and D adapted from Korner ; B adapted from Spyer ; C adapted from Loewy et al.


Figure 9.

Excitatory and inhibitory pathways regulating medullary pressor and depressor areas and preganglionic spinal sympathetic neurons (IML, IMM) and preganglionic medullary vagal neurons (VN). VRN, ventral reticular nuclei; A1, inhibitory noradrenergic neurons in ventral part of LRN; NE, norepinephrine; Ach, acetylcholine; Ms, skeletal muscle; Art. Baro., arterial baroreflex. Solid lines, pathways that stimulate neurons; dotted lines, pathways that suppress neurons.



Figure 10.

Activation of vagal neurons by anterior hypothalamus (Ant. Hypoth.) and NTS causing bradycardia (left) and inhibition of vagal neurons by the posterior hypothalamus (Post. Hypoth.) and by respiratory neurons causing tachycardia (right). V, respiratory neuronal activity that inhibits vagal neurons causing tachycardia; atropine blocks this inhibition.



Figure 11.

Electrical stimulation of diencephalon in decorticate paralyzed cats triggers simultaneously central hyperventilation (increased phrenic nerve activity) and increased motor activity of both biceps femoris nerves. Hyperventilation clearly does not depend on peripheral stimulus from contracting muscle or chemoreceptors.

From Eldridge et al.


Figure 12.

Cardiovascular responses to desynchronized sleep (means ± SE) before (solid lines) and after (dashed lines) sinoaortic denervation (6 episodes; 1 cat). Sleep induces hypotension, mesenteric vasodilatation, and iliac vasodilatation, but latter is reflexly buffered and reversed to vasoconstriction when baroreflexes are intact (solid lines). Sinoaortic denervation unmasks dilatation.

From Baccelli et al. , by permission of the American Heart Association


Figure 13.

A: carotid sinus blood pressure (BP), air flow, and single cardiac vagal efferent nerve (CVE) activity in dogs. Burst of firing caused by baroreceptor stimulation occurs only in expiration. B: effect of repeated brief baroreceptor stimulations by neck suction in humans (lower tracing) on RR interval (HP), during expiration (suctions 1, 3), and during inspiration (suctions 2, 4). Reflex bradycardia is greater during expiration.

A from Spyer ; B adapted from Trzebski et al.


Figure 14.

Excitatory neurons of vasomotor center (VMC) in brain stem [catecholaminergic (CA) or serotonergic (5‐HT)] may stimulate preganglionic neurons in IML to increase sympathetic activity and cause hypertension. Normally inhibited, these neurons are disinhibited by 1) decreased activity of inhibitory central CA nerves to VMC as in DOCA‐salt or renal hypertension, 2) decreased activity of arterial baroreceptor nerve or other central CA nerves to NTS, or 3) decreased activity of inhibitory CA nerves between NTS and VMC.

From Chalmers , by permission of the American Heart Association


Figure 15.

Stimulation of the carotid chemoreceptors with nicotine causes a reflex fall in coronary perfusion pressure (PP) and coronary vasodilatation during constant cardiac pacing and constant coronary blood flow (perfusion pump). Dilatation is not metabolic in view of the rise in coronary sinus O2 pressure (PO2). Atropine and vagotomy partially block it.

From Heistad and Abboud , by permission of the American Heart Association


Figure 16.

Activating carotid chemoreceptors by carotid hypoxemia causes hypertension, bradycardia, and reflex vasodilatation in paw and constriction in muscle. Paw and muscle perfused separately at constant blood flow. Carotid baroreceptor stimulation (BARO) in contrast causes hypotension, bradycardia, and vasodilatation in muscle and paw. SAP, systemic arterial pressure.

From Abboud et al. and Heistad, Abboud, et al.


Figure 17.

Dopamine (1 and 5 μg/kg−‐1/min) suppresses hyperventilatory response ( ) to hypoxia (10% O2) in humans. Minimal suppression during normoxia; none during hyperoxia, suggesting chemoreceptor mediation of dopamine action.

From Heistad and Abboud , by permission of the American Heart Association


Figure 18.

Blood flow to gracilis muscle (Grac. M.) and paw maintained constant with pump. During sustained stimulation of carotid sinus nerve (CSS), close to bulb to exclusively activate baroreceptor nerves, withdrawal of sympathetic tone caused reflex hypotension and dilatation in muscle and paw. Cyanide (CN) injected into ascending aorta during electrical stimulation of baroreceptors activated chemoreceptors, causing vasoconstriction in muscle and further dilatation in paw.

From Calvelo, Abboud, et al. , by permission of the American Heart Association


Figure 19.

Repeated brief (2‐min) carotid sinus nerve (CSN) stimulations (25 Hz, 0.5 ms, 0.25‐1.5 V; heavy horizontal lines), resulting in significant increases in phrenic nerve activity that outlast stimulus by up to 5 min of afterdischarge. Also inspiratory activity has long‐lasting increase (> 30 min) that becomes progressively larger with each stimulus and is blocked by intravenous methysergide (lower panel). Data normalized so highest value during stimulation equals 100 units. Partial CO2 pressure is 34 mmHg.

From Millhorn et al.


Figure 20.

Pressor responses to ischemic exercise in normal leg (solid line) and insensitive leg (dashed line) were similar. Ischemia of normal leg without exercise sustained pressor response, but ischemia of insensitive leg did not.

From Rowell et al. , by permission of the American Heart Association, adapted from Alam and Smirk


Figure 21.

Electrical lumbar nerve stimulation (0.1‐100 Hz) causes significant constriction in arterioles of gracilis muscle (solid lines) and hind paw (dashed lines) of dog, as indicated by marked increases in perfusion pressures at constant blood flow. Constriction is much more pronounced in venules and veins of paw than in muscle. In contrast to responses to direct nerve stimulation, reflex vasoconstrictor responses to chemoreceptor stimulation are selective to arterioles in muscle (Figs. , ). cps, Cycles per second.

From Calvelo, Abboud, et al. , by permission of the American Heart Association


Figure 22.

Changes in heart rate (HR) and renal and muscle resistances during stimulation of cardiac afferents (upper panels) and arterial baroreceptors (lower panels). Both sets of afferents are inhibitory with some selectivity. For example, cardiac afferents cause a significantly greater inhibition of renal resistance. Interactions between arterial baroreceptors and cardiac afferents and input from chemoreceptors and hypothalamic defense area cause a variety of responses. Variable interactions point to specificity in patterns of afferent convergence on various groups of brain stem neurons or connecting pathways. For example, chemoreceptor stimulation prevents cardiac afferents from inhibiting skeletal muscle resistance but does not influence inhibitory influence of arterial baroreceptors. (Schematic drawn from data in refs. ).



Figure 23.

Reduced forearm blood flow (Plethysmographic tracings in upper panels) and forearm volume at constant venous congesting pressure of 20 mmHg (lower panels) indicate increases in arteriolar resistances and venous tone, respectively. Responses are to intra‐arterial infusions of norepinephrine (left panels) and to lower‐body negative pressure (LBNP, −60 mmHg) sufficient to lower arterial pressure and pulse pressure (right panels). Arteriolar constriction was comparable with 2 interventions, but venous tone increase was negligible during LBNP compared to intra‐arterial NE.

From Abboud et al.


Figure 24.

Upnght tilt does not increase venous tone in calf of humans. Veins of limbs are not sensitive to arterial or cardiopulmonary baroreflexes, but arterioles are. Other venous segments, e.g., splanchnic veins, are sensitive to these baroreflexes, whereas veins of extremities are more sensitive to temperature or respiratory reflexes (cf. Fig. ).

From Abboud et al.


Figure 25.

Hyperventilatory response to stimulating carotid chemoreceptors with nicotine is augmented during systemic hypotension and inhibited during hypertension in anesthetized dogs. The rise in systemic arterial pressure suppresses base‐line ventilation, which tends to increase during hypotension.

From Heistad, Abboud, et al.


Figure 26.

Responses (means ± SE) to electrical stimulation of somatic afferents during volume expansion and after bilateral vagotomy (V). Volume expansion with +5, +10, and +15 ml/kg of 6% dextran in normal saline suppressed reflex renal vasoconstrictor response to electrical stimulation of somatic afferents in dogs with sinoaortic deafferentation as compared to control (C). Bilateral vagotomy markedly increased reflex vasoconstriction. Neither volume expansion nor vagotomy altered reflex increases in arterial pressure or heart rate.

From Thames and Abboud


Figure 27.

Effect of sequential denervation of carotid sinus nerves (C), aortic afferents (A), and vagi (V) in anesthetized rabbits. Means ± SE of increases in arterial pressure, perfusion pressure in the hindlimb (perfused at constant blood flow), and heart rate are shown. Denervation of carotid sinus nerves when aortic afferents are intact or after vagotomy causes much smaller increases in arterial pressure and perfusion pressure than their denervation after aortic afferents are cut. The same is true for aortic nerves before and after section of carotid sinus nerves and vagotomy. Also bilateral vagotomy causes much smaller increases in pressures when carotid and aortic afferents are intact than when they have been cut. These interactions are not apparent with respect to heart rate.



Figure 28.

Reflex changes in heart rate (upper panels) and in hindlimb perfusion pressure (lower panels) in anesthetized rabbits during changes in arterial pressure provoked with phenylephrine (PE) and nitroglycerin (NG). Solid lines, control responses; dashed lines, responses after section of carotid sinus nerves (CBRX; A panels) or aortic nerves (ABRX; B panels), or after sinoaortic denervation (SAD; C panels). Sectioning 1 set of afferents significantly reduces gain of baroreflex control of heart rate but not of hindlimb vascular resistance.

From Guo, Thames, and Abboud , by permission of the American Heart Association


Figure 29.

Left: effect of volume expansion with intravenous dextran in an anesthetized dog; integrated renal nerve activity declines. Right: correlations between changes in renal nerve activity (ΔRNA) and mean arterial pressure (ΔMAP) or mean pulmonary artery wedge pressure (PAW) during volume expansion. Sinoaortic denervation (SAD) had a minimal effect on changes in renal nerve activity, whereas bilateral vagotomy essentially abolished reflex.

From Abboud and Thames, Miller, and Abboud


Figure 30.

Left carotid sinus nerve activity decreases despite constant distending volume and isolated left carotid sinus pressure. Decrease resulted from a reflex triggered by distending right carotid sinus, causing withdrawal of sympathetic drive.

From Felder, Heesch, and Thames


Figure 31.

Responses (mean ± SE) of carotid sinus nerve activity during changes in carotid sinus pressure (Cvp, CN) before and after exposure of the carotid sinus to verapamil (VP; 5 μg/ml) or nifedipine (N; 10 μg/ml). *P < 0.05 for difference in slope of responses. (VP, 5 dogs; N, 6 dogs.)

From Heesch, Thames, and Abboud


Figure 32.

Activity of atrial vagal afferents during volume expansion in control dogs (solid line) and dogs in heart failure (dashed lines) in correlation to central venous pressure and left atrial pressure . The afferent activity is markedly impaired in heart failure.

Adapted from Greenberg et al , by permission of the American Heart Association, and Zucker et al.


Figure 33.

Interaction between somatic afferents and arterial and cardiopulmonary afferents. Reflex vasoconstrictor response to activating somatic afferents is augmented when inhibitory input for arterial and cardiopulmonary receptors is impaired.

From Abboud, Thames, and Mark


Figure 34.

Ouabain enhances atrial receptor discharge during volume expansion for similar levels of left atrial pressure (LAP) . Acetylstrophanthidin (AS) in coronary arteries enhances reflex inhibition of renal efferent nerve activity in anesthetized dogs for equivalent level of LAP. No inhibition is seen after bilateral vagotomy.

Adapted from Thames, Waickman, and Abboud and Zucker et al.


Figure 35.

Left panel: interaction between activity of cardiac vagal afferents and carotid baroreflex control of renal nerve activity in anesthetized dogs. Reduction in carotid sinus pressure in dogs with section of the aortic depressor nerves causes significant increases in renal nerve activity Reflex gain in bar graphs (means ± SE of renal nerve activity change in Hz per unit change in arterial pressure) declines significantly during occlusion of circumflex (Cx) but not during occlusion of left anterior descending arteries (LAD). After bilateral vagotomy, gain is markedly enhanced and Cx and LAD occlusion have no effect on the gain.

Data from Abboud and Waickman and Abboud
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Francois M. Abboud, Marc D. Thames. Interaction of Cardiovascular Reflexes in Circulatory Control. Compr Physiol 2011, Supplement 8: Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow: 675-753. First published in print 1983. doi: 10.1002/cphy.cp020319