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Cardiovascular Reflex Control by Afferent Fibers from Skeletal Muscle Receptors

Jere H. Mitchell, Robert F. Schmidt

10.1002/cphy.cp020317

Source: Supplement 8: Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow

Originally published: 1983

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Afferent Fibers from Skeletal Muscle and Their Receptors
1.1 Composition of Muscle Nerves
1.2 Muscle Spindles and Golgi Tendon Organs
1.3 Receptive Properties of Group III and Group IV Afferent Fibers
2 Central Pathways for Cardiovascular Reflexes from Skeletal Muscle Receptors
2.1 Spinal Termination of Primary Muscle Afferents
2.2 Central Pathways Arising From Myelinated Primary Muscle Afferents
2.3 Central Pathways Arising From Unmyelinated Primary Muscle Afferents
2.4 Ascending and Descending Spinal Pathways Involved in Cardiovascular Reflex Control From Skeletal Muscle
3 Organization of Efferent Outflow in Pre‐ and Postganglionic Neurons
4 Cardiovascular Responses from Skeletal Muscle Receptors
4.1 Effect of Activation of Afferent Fibers
4.2 Effect of Induced Muscular Contraction (Simulated Exercise)
5 Interaction of Muscle Afferents with Other Cardiovascular Reflexes
5.1 Arterial Baroreceptors
5.2 Cardiopulmonary Vagal Afferents
6 Role of Skeletal Muscle Afferents in Cardiovascular Response to Exercise in Humans
6.1 Dynamic and Static Exercise
6.2 Central Control (Central Command)
6.3 Peripheral Control
6.4 Integration of Neural Control Mechanisms During Exercise
7 Conclusion
Figure 1. Figure 1.

Experimental arrangements to record, identify, and stimulate fine afferent units of skeletal muscle and tendon.
Figure 2. Figure 2.

Responses of gastrocnemius‐soleus fine afferent units to stretch. Peristimulus time histograms plotted from computer records with a dwell time of 1‐4s for each address. Filled bars, hindpaw held flexed (static stretch); open bars, paw moved rhythmically from extended to flexed position at a rate of 1 Hz (dynamic stretch). A and B: group IV units (conduction velocities 0.9 and 2.1 m/s, respectively). C, D, and E: group III units (conduction velocities 21.5, 16.1, and 15.9 m/s). F: stretch‐sensitive (excitation) units excited by static and/or dynamic stretch.

From Mense 203
Figure 3. Figure 3.

Responses of gastrocnemius‐soleus fine afferent units to isometric contractions induced by stimulating these muscle nerves every second with a 50‐Hz tetanus lasting 500 ms for 2 min. Muscle temperature changes thus induced are also displayed. Histograms give resulting discharges at an address advance rate of 1/4 s. A: group III unit (conduction velocity 14.2 m/s) probably activated mechanically (CSm unit). B: responses to stretch of this group III unit. C: group IV unit (conduction velocity 0.9 m/s), probably not activated mechanically (CSx unit). Unit was not sensitive to stretch. No appreciable change in response pattern occurred after occlusion of local blood supply. D: group IV unit (conduction velocity 0.7 m/s) responds preferentially during ischemic contractions (N unit).

From Mense 203
Figure 4. Figure 4.

Responses of gastrocnemius‐soleus group IV unit (conduction velocity 1.1 m/s) to temperature stimuli. Inset in C: peak discharge to a warm stimulus. Brad., bradykinin; 5‐HT, serotonin.

From Mense 203
Figure 5. Figure 5.

Activity in a single group IV afferent unit in response to intra‐arterial injection of various algesic agents. Recording from gastrocnemius part of sciatic nerve at upper part of thigh. Conduction velocity of fiber was 1.27 m/s. Arrows, intra‐arterial injections. Brad., bradykinin; Hist., histamine; 5‐HT, serotonin. Upper right‐hand inset shows receptor discharge after 5‐HT injection.

Adapted from Mense and Schmidt 205
Figure 6. Figure 6.

Response characteristics of a group III afferent unit having a receptive field in the calcaneal tendon. Inset: area from which unit could be activated by stroking and touching with a painter's brush is hatched. Mod. P., moderate, innocuous pressure; Nox. P., noxious pressure resulting in tissue damage; Stretch, muscle and tendon rapidly stretched and kept in stretched position for 15 s; Contraction, 1 tetanic contraction of 0.5 s duration every second, induced by electrical stimulation of the muscle nerve. Force of 2 kp was maximal here because muscle was not prestretched. Thermal stimulation was applied via water‐perfused thermodes in contact with receptive field. Conduction velocity of the afferent fiber was 8.8 m/s.

S. Mense and H. Meyer, unpublished observations
Figure 7. Figure 7.

Organization of vasoconstrictor systems and sudomotor system in brain‐intact animals (supraspinal and spinal) and in spinal animals (spinal) with respect to various afferent input systems. Baro, stimulation of arterial baroreceptors; Chemo, stimulation of arterial chemoreceptors; Noci, stimulation of cutaneous nociceptors (i.l., ipsilateral; c.l., contralateral); Vibr., stimulation of Pacinian corpuscles by vibration; Warm, stimulation of warm receptors in the spinal canal; Air jet, stimulation of hair follicle receptors.

Adapted from Jänig 128
Figure 8. Figure 8.

Specificity of sympathetic channels supplying peripheral target organs in skin and muscle of cat's hindlimb and tail. Deduced from reflex reaction patterns summarized in Fig. 7.

From Jänig and Szulczyk 135
Figure 9. Figure 9.

Blood pressure responses to stimulation of afferent fibers from muscle. Stimulation at 12 V for 0.5 ms at 6 Hz (A), at 20 Hz (B), and at 100 Hz (C).

From Johansson 136
Figure 10. Figure 10.

Percent change from control of cardiovascular and respiratory responses to capsaicin infusion into skeletal muscles and to induced isometric exercise. HR, heart rate; MAP, mean arterial pressure; CO, cardiac output; MV, respiratory minute volume; TPR, total peripheral vascular resistance.

From Crayton, Mitchell, and Payne 70
Figure 11. Figure 11.

Effect of somatopressor reflex on coronary artery resistance. A: control; B: after propranolol and at constant heart rate. COR, mean perfusion pressure of a constantly perfused coronary artery; SAP, mean systemic arterial pressure; HR, heart rate. Black bars, stimulation.

From Nutter and Wickliffe 218, by permission of the American Heart Association, Inc
Figure 12. Figure 12.

Percent change from control of cardiac output and organ blood flow to capsaicin infusion into skeletal muscles and into induced isometric exercise.

From Crayton, Mitchell, and Payne 70
Figure 13. Figure 13.

Effect of somatopressor reflex on venous tone. Vein, mean perfusion pressure in the lateral saphenous vein perfused at constant flow; SAP, mean systemic arterial pressure; HR, heart rate. Black bar, stimulation of central end of sectioned tibial nerve.

From Nutter and Wickliffe 218, by permission of the American Heart Association, Inc
Figure 14. Figure 14.

Response to induced static exercise. LVP, left ventricular pressure; dP/dt, rate of left ventricular pressure development. Time mark, 1 s. Exercise between bars.

From Mitchell et al. 212
Figure 15. Figure 15.

Effect of muscle paralysis on changes in mean aortic pressure and perfusion pressure in left paw and lateral saphenous vein during induced rhythmic contractions (upper panels) and during sustained contractions (lower panels) before and after muscle paralysis produced by gallamine.

From Clement and Shepherd 52, by permission of the American Heart Association, Inc
Figure 16. Figure 16.

Cardiovascular response to induced exercise. AP, arterial pressure; HPP, hindlimb perfusion pressure; HR, heart rate. A: dynamic exercise; B: static exercise induced by stimulation of femoral nerve.

From Tallarida et al. 265
Figure 17. Figure 17.

Effect of arterial occlusion on arterial blood presure response during induced exercise. • Static exercise without occlusion; ○, static exercise with occlusion; ⋄, dynamic exercise without occlusion; ⋄, dynamic exercise with occlusion. Arrows, pairs of consecutive contractions with free and occluded arterial inflow.

From Pérez‐González 225, by permission of the American Heart Association, Inc
Figure 18. Figure 18.

Relation of rate of left ventricular pressure development to left ventricular pressure at rest and during induced static exercise before and after blockade of β‐adrenergic receptor.

From Mitchell et al. 212
Figure 19. Figure 19.

Regional myocardial blood flow and resistance responses to induced static exercise after blockade of β‐adrenergic receptor with propranolol.

From Longhurst, Aung‐Din, and Mitchell 186
Figure 20. Figure 20.

Response to induced static exercise during anodal block. Records of tidal volume (VT), arterial blood pressure (B.P.), and dorsal root compound action potentials are shown for 3 exercise responses. Upper panel, control exercise response before anodal block; middle panel, exercise response during anodal block just sufficient to abolish the A wave of compound action potential; lower panel, control exercise response after removal of anodal block.

From McCloskey and Mitchell 198
Figure 21. Figure 21.

Response to induced static exercise during anesthetic block. VT tidal volume; B.P., arterial blood pressure. Upper panel, control exercise response before anesthetic block; middle panel, exercise response during anesthetic block that had not affected the A wave of the compound action potential; lower panel, control exercise response after removal of the anesthetic block.

From McCloskey and Mitchell 198
Figure 22. Figure 22.

Blood pressure response to induced contractions of cat medial gastrocnemius muscle after partial neuromuscular blockade. ○, Systolic blood pressure; •, diastolic blood pressure recorded before, during, and after fatiguing contraction. Solid lines, after administration of curare; dashed lines, after administration of decamethonium.

From Petrofsky and Lind 228
Figure 23. Figure 23.

Baroreflex activity in a dog. ○, Points for pulse interval at rest; •, pulse interval during induced isometric contractions (exercise) of hindlimb muscles. Points are plotted at a control level of blood pressure and at the peak of rise in blood pressure caused by inflating a balloon in the thoracic aorta. Slopes of lines joining pairs of points represent baroreceptor‐cardiodepressor reflex sensitivity.

From Streatfeild et al. 261, by permission of the New England Journal of Medicine
Figure 24. Figure 24.

Heart rate, mean blood pressure, smoothed, rectified electromyographic activity (SREMG), and force during 5 min of static contraction (mean values). ⋄, Force‐constant experiments; ×, SREMG‐constant experiments. • Significantly different values obtained for mean blood pressure and heart rate in 2 series of experiments (P < 0.01 after 1.5 and 2 min of contraction, respectively).

From Schibye et al. 249


Figure 1.

Experimental arrangements to record, identify, and stimulate fine afferent units of skeletal muscle and tendon.



Figure 2.

Responses of gastrocnemius‐soleus fine afferent units to stretch. Peristimulus time histograms plotted from computer records with a dwell time of 1‐4s for each address. Filled bars, hindpaw held flexed (static stretch); open bars, paw moved rhythmically from extended to flexed position at a rate of 1 Hz (dynamic stretch). A and B: group IV units (conduction velocities 0.9 and 2.1 m/s, respectively). C, D, and E: group III units (conduction velocities 21.5, 16.1, and 15.9 m/s). F: stretch‐sensitive (excitation) units excited by static and/or dynamic stretch.

From Mense 203


Figure 3.

Responses of gastrocnemius‐soleus fine afferent units to isometric contractions induced by stimulating these muscle nerves every second with a 50‐Hz tetanus lasting 500 ms for 2 min. Muscle temperature changes thus induced are also displayed. Histograms give resulting discharges at an address advance rate of 1/4 s. A: group III unit (conduction velocity 14.2 m/s) probably activated mechanically (CSm unit). B: responses to stretch of this group III unit. C: group IV unit (conduction velocity 0.9 m/s), probably not activated mechanically (CSx unit). Unit was not sensitive to stretch. No appreciable change in response pattern occurred after occlusion of local blood supply. D: group IV unit (conduction velocity 0.7 m/s) responds preferentially during ischemic contractions (N unit).

From Mense 203


Figure 4.

Responses of gastrocnemius‐soleus group IV unit (conduction velocity 1.1 m/s) to temperature stimuli. Inset in C: peak discharge to a warm stimulus. Brad., bradykinin; 5‐HT, serotonin.

From Mense 203


Figure 5.

Activity in a single group IV afferent unit in response to intra‐arterial injection of various algesic agents. Recording from gastrocnemius part of sciatic nerve at upper part of thigh. Conduction velocity of fiber was 1.27 m/s. Arrows, intra‐arterial injections. Brad., bradykinin; Hist., histamine; 5‐HT, serotonin. Upper right‐hand inset shows receptor discharge after 5‐HT injection.

Adapted from Mense and Schmidt 205


Figure 6.

Response characteristics of a group III afferent unit having a receptive field in the calcaneal tendon. Inset: area from which unit could be activated by stroking and touching with a painter's brush is hatched. Mod. P., moderate, innocuous pressure; Nox. P., noxious pressure resulting in tissue damage; Stretch, muscle and tendon rapidly stretched and kept in stretched position for 15 s; Contraction, 1 tetanic contraction of 0.5 s duration every second, induced by electrical stimulation of the muscle nerve. Force of 2 kp was maximal here because muscle was not prestretched. Thermal stimulation was applied via water‐perfused thermodes in contact with receptive field. Conduction velocity of the afferent fiber was 8.8 m/s.

S. Mense and H. Meyer, unpublished observations


Figure 7.

Organization of vasoconstrictor systems and sudomotor system in brain‐intact animals (supraspinal and spinal) and in spinal animals (spinal) with respect to various afferent input systems. Baro, stimulation of arterial baroreceptors; Chemo, stimulation of arterial chemoreceptors; Noci, stimulation of cutaneous nociceptors (i.l., ipsilateral; c.l., contralateral); Vibr., stimulation of Pacinian corpuscles by vibration; Warm, stimulation of warm receptors in the spinal canal; Air jet, stimulation of hair follicle receptors.

Adapted from Jänig 128


Figure 8.

Specificity of sympathetic channels supplying peripheral target organs in skin and muscle of cat's hindlimb and tail. Deduced from reflex reaction patterns summarized in Fig. 7.

From Jänig and Szulczyk 135


Figure 9.

Blood pressure responses to stimulation of afferent fibers from muscle. Stimulation at 12 V for 0.5 ms at 6 Hz (A), at 20 Hz (B), and at 100 Hz (C).

From Johansson 136


Figure 10.

Percent change from control of cardiovascular and respiratory responses to capsaicin infusion into skeletal muscles and to induced isometric exercise. HR, heart rate; MAP, mean arterial pressure; CO, cardiac output; MV, respiratory minute volume; TPR, total peripheral vascular resistance.

From Crayton, Mitchell, and Payne 70


Figure 11.

Effect of somatopressor reflex on coronary artery resistance. A: control; B: after propranolol and at constant heart rate. COR, mean perfusion pressure of a constantly perfused coronary artery; SAP, mean systemic arterial pressure; HR, heart rate. Black bars, stimulation.

From Nutter and Wickliffe 218, by permission of the American Heart Association, Inc


Figure 12.

Percent change from control of cardiac output and organ blood flow to capsaicin infusion into skeletal muscles and into induced isometric exercise.

From Crayton, Mitchell, and Payne 70


Figure 13.

Effect of somatopressor reflex on venous tone. Vein, mean perfusion pressure in the lateral saphenous vein perfused at constant flow; SAP, mean systemic arterial pressure; HR, heart rate. Black bar, stimulation of central end of sectioned tibial nerve.

From Nutter and Wickliffe 218, by permission of the American Heart Association, Inc


Figure 14.

Response to induced static exercise. LVP, left ventricular pressure; dP/dt, rate of left ventricular pressure development. Time mark, 1 s. Exercise between bars.

From Mitchell et al. 212


Figure 15.

Effect of muscle paralysis on changes in mean aortic pressure and perfusion pressure in left paw and lateral saphenous vein during induced rhythmic contractions (upper panels) and during sustained contractions (lower panels) before and after muscle paralysis produced by gallamine.

From Clement and Shepherd 52, by permission of the American Heart Association, Inc


Figure 16.

Cardiovascular response to induced exercise. AP, arterial pressure; HPP, hindlimb perfusion pressure; HR, heart rate. A: dynamic exercise; B: static exercise induced by stimulation of femoral nerve.

From Tallarida et al. 265


Figure 17.

Effect of arterial occlusion on arterial blood presure response during induced exercise. • Static exercise without occlusion; ○, static exercise with occlusion; ⋄, dynamic exercise without occlusion; ⋄, dynamic exercise with occlusion. Arrows, pairs of consecutive contractions with free and occluded arterial inflow.

From Pérez‐González 225, by permission of the American Heart Association, Inc


Figure 18.

Relation of rate of left ventricular pressure development to left ventricular pressure at rest and during induced static exercise before and after blockade of β‐adrenergic receptor.

From Mitchell et al. 212


Figure 19.

Regional myocardial blood flow and resistance responses to induced static exercise after blockade of β‐adrenergic receptor with propranolol.

From Longhurst, Aung‐Din, and Mitchell 186


Figure 20.

Response to induced static exercise during anodal block. Records of tidal volume (VT), arterial blood pressure (B.P.), and dorsal root compound action potentials are shown for 3 exercise responses. Upper panel, control exercise response before anodal block; middle panel, exercise response during anodal block just sufficient to abolish the A wave of compound action potential; lower panel, control exercise response after removal of anodal block.

From McCloskey and Mitchell 198


Figure 21.

Response to induced static exercise during anesthetic block. VT tidal volume; B.P., arterial blood pressure. Upper panel, control exercise response before anesthetic block; middle panel, exercise response during anesthetic block that had not affected the A wave of the compound action potential; lower panel, control exercise response after removal of the anesthetic block.

From McCloskey and Mitchell 198


Figure 22.

Blood pressure response to induced contractions of cat medial gastrocnemius muscle after partial neuromuscular blockade. ○, Systolic blood pressure; •, diastolic blood pressure recorded before, during, and after fatiguing contraction. Solid lines, after administration of curare; dashed lines, after administration of decamethonium.

From Petrofsky and Lind 228


Figure 23.

Baroreflex activity in a dog. ○, Points for pulse interval at rest; •, pulse interval during induced isometric contractions (exercise) of hindlimb muscles. Points are plotted at a control level of blood pressure and at the peak of rise in blood pressure caused by inflating a balloon in the thoracic aorta. Slopes of lines joining pairs of points represent baroreceptor‐cardiodepressor reflex sensitivity.

From Streatfeild et al. 261, by permission of the New England Journal of Medicine


Figure 24.

Heart rate, mean blood pressure, smoothed, rectified electromyographic activity (SREMG), and force during 5 min of static contraction (mean values). ⋄, Force‐constant experiments; ×, SREMG‐constant experiments. • Significantly different values obtained for mean blood pressure and heart rate in 2 series of experiments (P < 0.01 after 1.5 and 2 min of contraction, respectively).

From Schibye et al. 249
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Article Title: Cardiovascular Reflex Control by Afferent Fibers from Skeletal Muscle Receptors
 

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Jere H. Mitchell, Robert F. Schmidt. Cardiovascular Reflex Control by Afferent Fibers from Skeletal Muscle Receptors. Compr Physiol 2011, Supplement 8: Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow: 623-658. First published in print 1983. doi: 10.1002/cphy.cp020317