Comprehensive Physiology Wiley Online Library

Central Neural Control of Respiration and Circulation During Exercise

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Respiration
2 Circulation
3 Central Command Mechanisms
3.1 Central Drive of Locomotion
3.2 Locomotor Pattern Generator
3.3 Supraspinal Locomotor Sites
4 Central Command Control of Respiration and Circulation in Animals
4.1 Cerebral Cortex
4.2 Hypothalamic Locomotor Region
4.3 Mesencephalic Locomotor Region
4.4 Amygdala
4.5 Awake, Exercising Animal Studies
5 Short‐Term Potentiation
5.1 Respiration
6 Central Command Control of Respiration and Circulation in Humans
6.1 Respiration
6.2 Circulation
7 Interactions Between Central Command and Peripheral Feedback
8 Interaction of Central Command with Cardiorespiratory Reflexes
8.1 Baroreceptor Reflex
8.2 Hering‐Breuer Reflex
8.3 Chemoreceptor Reflexes
9 Conclusions
Figure 1. Figure 1.

Ventilation (V) increases in direct proportion to the workload during mild and moderate rhythmic exercise in humans such that arterial PO2, PCO2, and pH remain constant.

From Waldrop
Figure 2. Figure 2.

Examples of cardiovascular responses to (A) dynamic and (B) static exercise. The dynamic exercise was progressively increased to ; the static exercise was sustained at 30% of maximal voluntary contraction. Q, cardiac output; HR, heart rate; SV, stroke volume; ABP, systolic (top line), mean (middle line), and diastolic (bottom line) arterial blood pressure; TPR, total peripheral resistance.

From Mitchell and Raven
Figure 3. Figure 3.

Frontal and parasagittal drawings showing location of hypothalamic (subthalamic) and mesencephalic locomotor regions in the cat.

Adapted from Eldridge et al.
Figure 4. Figure 4.

Animal preparations utilized for studying exercise in the unanesthetized decorticate cat (A) and fictive locomotion in the paralyzed ventilated cat (B).

Adapted from Eldridge et al.
Figure 5. Figure 5.

Example of the respiratory, cardiovascular, and fictive locomotor responses elicited by stimulation in the hypothalamic locomotor region of a paralyzed cat.

From Eldridge et al.
Figure 6. Figure 6.

Hemodynamic and respiratory responses to electrical stimulation of the hypothalamic (subthalamic) locomotor region.

From Waldrop et al.
Figure 7. Figure 7.

Averaged changes in blood flow (as determined using the radioactive microsphere technique) to the heart, kidneys, diaphragm, and selected limb muscles of anesthetized cats during stimulation of the hypothalamic locomotor region.

From Waldrop et al.
Figure 8. Figure 8.

Responses (electromyographic recordings) of the triceps muscles to microinje GABA antagonists (A, picrotoxin; B, bicuculline) and a GABA agonist (muscimol) into pothalamic locomotor region of an anesthetized cat. Both antagonists produced rhythm nating bursts of left and right triceps activity that were reversed by the GABA agonist. 1 of the injections are denoted by filled triangles in C and D.

From Waldrop et al.
Figure 9. Figure 9.

Arterial pressure, heart rate, and skeletal muscle (triceps) responses to microinjection of a GABA antagonist [bicuculline methiodide (BMI)] into the hypothalamic locomotor region of an anesthetized cat. The responses evoked by the GABA antagonist were reversed by microinjection of a GABA agonist (muscimol) into the same hypothalamic site. The injection site is denoted by a filled triangle on the line drawing.

From Waldrop et al.
Figure 10. Figure 10.

Arterial pressure, heart rate, and sympathetic nerve (cervical nerve activity) responses to microinjection of a GABA antagonist (picrotoxin) into the hypothalamic locomotor region of an anesthetized cat. The increased activity (B) elicited by the injection was reversed by microinjection of a GABA agonist

muscimol, (C)]. [From Waldrop and Bauer
Figure 11. Figure 11.

Averaged changes in force, mean renal sympathetic nerve activity (MRNA), heart rate (HR), and mean arterial blood pressure (MAP) during two bouts of static exercise performed by a conscious cat.

From Matsukawa et al.
Figure 12. Figure 12.

Recording of phrenic nerve and integrated phrenic activity during control (left), during stimulation (bar) of a carotid sinus nerve, and during recovery in a paralyzed, vagotomized cat with partial pressures of CO2 and O2 kept constant by means of a servocontrolled ventilator. It shows the rapid increase of respiration at stimulus onset, further increase to a steady‐state within two breaths, and a rapid decrease on stimulus cessation followed by a slow recovery process (afterdischarge).

Figure 13. Figure 13.

Example of development and recovery of respiratory short‐term potentiation with stimulation of calf muscles (CM) in paralyzed, vagotomized cat with controlled PCO2. The animal had fortuitously developed apneustic breathing. The potentiation develops and decays according to its usual time course and is independent of the actual respirations.

Figure 14. Figure 14.

Effects of different modes of stimulating carotid sinus nerve on respiratory (phrenic) responses and recovery in paralyzed, vagotomized cat. A, Continuous stimulation. B, Expiratory‐only stimulation. C, Alternate‐cycle stimulation. Stimulated breaths of alternate‐cycle experiment are similar to those of continuous stimulation, and nonstimulated breaths are similar to those of expiratory stimulation. Despite differences in direct effects of stimulus, the amount of potentiation and the decay (afterdischarge) patterns are similar in all three experiments. Slowly rising activity during expiratory‐only stimulations represents increasing activation of potentiation. AP, arterial pressure.

From Eldridge and Gill‐Kumar
Figure 15. Figure 15.

Experiments showing that complete suppression of inspiratory activity during carotid sinus nerve (CSN) stimulation does not prevent potentiation in paralyzed, vagotomized cat. A, Control experiment showing baseline activity at left, effect of CSN stimulation of 30 s, and recovery. B, Baseline activity at left, effect of combined CSN and vagal stimulation, and recovery. Although inspirations are completely inhibited by vagal effects during combined stimulation, poststimulation respiratory activity is augmented, just as in control experiment, and decays with approximately the same time course.

From Eldridge and Gill‐Kumar
Figure 16. Figure 16.

Semilogarithmic plot of respiratory activity (units) vs. time during a stimulation (STIM.) and decay of potentiation (AFTERDISCHARGE) to show potential error in measurement of its time constant (τ). The true τ of the decay is 50 s. If the τ is measured as the 63% decay from the true starting level of 50 units, it will give the correct value of 50 s (point A). However, some of the total decrease, the loss of the direct effect of the stimulus, is not part of the exponential function. Thus, if the τ is measured as a 63% decay from the end‐stimulation level of 100 units, then an incorrect τ of only 15.3 s (point B) will be calculated.

Figure 17. Figure 17.

Computer‐generated neural inspiratory (phrenic equivalent) activity in a model that incorporates short‐term potentiation (onset τ, 10 s; offset τ, 50 s) and that mimicks constant blood gases and has no other feedback. Control at left, then a 4 min facilitatory stimulus (bar), and then 5 min of recovery. The STP has almost no effect on the pattern after the first 30 s of stimulation and little effect on the recovery after 2 min. (The irregular patterns in the tracing are pixel effects from the computer screen and have no physiological meaning.)

Figure 18. Figure 18.

Computer‐generated ventilation (liters per minute) and arterial, end‐tidal, and medullary PCO2 during rest (VO2 = 0.25 liter/min), 6 min of exercise ( = 1.0 liter/min), and recovery (see text and footnote for details of model). In panel A the model includes the usual short‐term potentiating (STP) mechanism (τ on = 10 s; τ off = 50 s); it yields a typical and normal ventilatory response to exercise. In panel B the STP has been removed, with the result that ventilation at the end of the 6 min of exercise is slightly less than in the model with STP, all PCO2 values are slightly higher, and there are increased oscillations of ventilation after both onset and cessation of exercise.

Figure 19. Figure 19.

Schematic representation of the ventilatory response to static (handgrip) exercise. Asterisks denote the onset and end of the exercise bout.

From Waldrop
Figure 20. Figure 20.

A, Experimental design for reducing the magnitude of central command required to achieve a muscle tension. The drawing shows how vibration is used to activate primary afferents from the contracting muscles, thereby contributing reflex excitation of the motoneurons innervating the muscle. The same amount of force can be generated as was true without the reflex excitation (on the left) but with a reduced central command component. B, Experimental design for increasing the magnitude of central command required to achieve a muscle tension. The drawing shows how vibration is used to activate primary afferents from a muscle (biceps) antagonist to the contracting muscles, thereby contributing reflex inhibition of the motoneurons innervating the contracting muscle. An increased central command component is required in order for the same amount of force to be generated as was true without the reflex inhibition (on the left).

Adapted from Goodwin et al.
Figure 21. Figure 21.

A, Reduction of central command. The blood pressure, heart rate, and ventilatory responses during a normal contraction are shown by the filled circles and continuous lines; the responses when vibration was used to reduce central command are shown by open circles and interrupted lines. B, Augmentation of central command. The blood pressure, heart rate, and ventilatory responses during a normal contraction are shown by the filled circles and continuous lines; the responses when vibration was used to increase central command are shown by open circles and interrupted lines.

Adapted from Goodwin et al.
Figure 22. Figure 22.

Schematic representation of the ventilatory response to static (handgrip) exercise. Asterisks denote the onset and end of the exercise bout.

From Waldrop
Figure 23. Figure 23.

Effect on heart rate and blood pressure responses to static exercise of neuromuscular blockade and of epidural anesthesia. Left, Comparison of each intervention to control at the same absolute force. Right, Comparison at the same relative force.

From Mitchell et al.
Figure 24. Figure 24.

Effect of intended contraction on heart rate and blood pressure in a totally paralyzed subject. Bars indicate the time when contractions were attempted with values for percentage of MVC.

From Gandevia et al.
Figure 25. Figure 25.

Heart rate and blood pressure responses and rating of perceived exertion (r.p.e. units on scale of 6–20) during progressive exercise to maximal. Filled circles represent exercise during the control study and open circles represent maximal effort as the neuromuscular blockade decreased. Values are means ± SEM.

From Galbo et al.
Figure 26. Figure 26.

Muscle sympathetic nerve activity (MSNA) and force. % MVC, percentage of maximal voluntary contraction. A study from one subject before and during partial neuromuscular blockade with curare.

From Victor et al.
Figure 27. Figure 27.

Effect of muscle fatigue on rating of perceived effort (RPE) and peak increase in skin sympathetic nerve activity [Skin SNA (%)] of the same handgrip force (kg). Data are mean ± SEM. Asterisks denote significant differences from previous handgrip contraction (P < 0.05).

From Vissing et al.
Figure 28. Figure 28.

Hemodynamic values at rest and during work rates of 10, 20, and 30 watts (W) performed with one leg and 2 × 20 W performed with two legs. Open circles represent voluntary dynamic exercise, filled triangles represent electrically induced exercise, and filled rectangles represent electrically induced exercise during epidural anesthesia. Values are mean ± SEM. Asterisk denotes differences between voluntary and electrically induced exercise before epidural anesthesia. Double asterisks denote differences between electrically induced exercise with and without epidural anesthesia.

From Strange et al.
Figure 29. Figure 29.

Cardiac output, heart rate, stroke volume, and blood pressure at rest and during one‐legged exercise at two workloads. Upper three panels in normal subjects with no weakness. (A, right leg; Δ, left leg). Lower four panels in subjects with one weak leg (•, normal leg; τ, weak leg). Values are means (± SD).

From Innes et al.
Figure 30. Figure 30.

Effects of static muscular contraction (elicited by ventral root stimulation) upon arterial pressure, heart rate, and the discharge frequency of a posterior hypothalamic neuron of an anesthetized cat. Note that contraction and other mechanical stimulation of the gastrocnemius muscles increased the discharge frequency of this neuron. Baroreceptor stimulation produced by a phenylephrine‐induced increase in arterial pressure had no significant effect upon this neuron. Location of the neuron is indicated by the filled triangle in the line drawing at bottom.

From Waldrop and Stremel
Figure 31. Figure 31.

Computer‐generated ventilatory and PCO2 responses to dynamic exercise. Panel A shows the normal responses with all mechanisms present. In panel B, only the central command component has been deleted. Notice the loss of the initial fast respiratory component but with the peak response differing little from that observed in panel A. The respiratory response is now dependent upon the rising PCO2. Details of the computer model are described in the text.



Figure 1.

Ventilation (V) increases in direct proportion to the workload during mild and moderate rhythmic exercise in humans such that arterial PO2, PCO2, and pH remain constant.

From Waldrop


Figure 2.

Examples of cardiovascular responses to (A) dynamic and (B) static exercise. The dynamic exercise was progressively increased to ; the static exercise was sustained at 30% of maximal voluntary contraction. Q, cardiac output; HR, heart rate; SV, stroke volume; ABP, systolic (top line), mean (middle line), and diastolic (bottom line) arterial blood pressure; TPR, total peripheral resistance.

From Mitchell and Raven


Figure 3.

Frontal and parasagittal drawings showing location of hypothalamic (subthalamic) and mesencephalic locomotor regions in the cat.

Adapted from Eldridge et al.


Figure 4.

Animal preparations utilized for studying exercise in the unanesthetized decorticate cat (A) and fictive locomotion in the paralyzed ventilated cat (B).

Adapted from Eldridge et al.


Figure 5.

Example of the respiratory, cardiovascular, and fictive locomotor responses elicited by stimulation in the hypothalamic locomotor region of a paralyzed cat.

From Eldridge et al.


Figure 6.

Hemodynamic and respiratory responses to electrical stimulation of the hypothalamic (subthalamic) locomotor region.

From Waldrop et al.


Figure 7.

Averaged changes in blood flow (as determined using the radioactive microsphere technique) to the heart, kidneys, diaphragm, and selected limb muscles of anesthetized cats during stimulation of the hypothalamic locomotor region.

From Waldrop et al.


Figure 8.

Responses (electromyographic recordings) of the triceps muscles to microinje GABA antagonists (A, picrotoxin; B, bicuculline) and a GABA agonist (muscimol) into pothalamic locomotor region of an anesthetized cat. Both antagonists produced rhythm nating bursts of left and right triceps activity that were reversed by the GABA agonist. 1 of the injections are denoted by filled triangles in C and D.

From Waldrop et al.


Figure 9.

Arterial pressure, heart rate, and skeletal muscle (triceps) responses to microinjection of a GABA antagonist [bicuculline methiodide (BMI)] into the hypothalamic locomotor region of an anesthetized cat. The responses evoked by the GABA antagonist were reversed by microinjection of a GABA agonist (muscimol) into the same hypothalamic site. The injection site is denoted by a filled triangle on the line drawing.

From Waldrop et al.


Figure 10.

Arterial pressure, heart rate, and sympathetic nerve (cervical nerve activity) responses to microinjection of a GABA antagonist (picrotoxin) into the hypothalamic locomotor region of an anesthetized cat. The increased activity (B) elicited by the injection was reversed by microinjection of a GABA agonist

muscimol, (C)]. [From Waldrop and Bauer


Figure 11.

Averaged changes in force, mean renal sympathetic nerve activity (MRNA), heart rate (HR), and mean arterial blood pressure (MAP) during two bouts of static exercise performed by a conscious cat.

From Matsukawa et al.


Figure 12.

Recording of phrenic nerve and integrated phrenic activity during control (left), during stimulation (bar) of a carotid sinus nerve, and during recovery in a paralyzed, vagotomized cat with partial pressures of CO2 and O2 kept constant by means of a servocontrolled ventilator. It shows the rapid increase of respiration at stimulus onset, further increase to a steady‐state within two breaths, and a rapid decrease on stimulus cessation followed by a slow recovery process (afterdischarge).



Figure 13.

Example of development and recovery of respiratory short‐term potentiation with stimulation of calf muscles (CM) in paralyzed, vagotomized cat with controlled PCO2. The animal had fortuitously developed apneustic breathing. The potentiation develops and decays according to its usual time course and is independent of the actual respirations.



Figure 14.

Effects of different modes of stimulating carotid sinus nerve on respiratory (phrenic) responses and recovery in paralyzed, vagotomized cat. A, Continuous stimulation. B, Expiratory‐only stimulation. C, Alternate‐cycle stimulation. Stimulated breaths of alternate‐cycle experiment are similar to those of continuous stimulation, and nonstimulated breaths are similar to those of expiratory stimulation. Despite differences in direct effects of stimulus, the amount of potentiation and the decay (afterdischarge) patterns are similar in all three experiments. Slowly rising activity during expiratory‐only stimulations represents increasing activation of potentiation. AP, arterial pressure.

From Eldridge and Gill‐Kumar


Figure 15.

Experiments showing that complete suppression of inspiratory activity during carotid sinus nerve (CSN) stimulation does not prevent potentiation in paralyzed, vagotomized cat. A, Control experiment showing baseline activity at left, effect of CSN stimulation of 30 s, and recovery. B, Baseline activity at left, effect of combined CSN and vagal stimulation, and recovery. Although inspirations are completely inhibited by vagal effects during combined stimulation, poststimulation respiratory activity is augmented, just as in control experiment, and decays with approximately the same time course.

From Eldridge and Gill‐Kumar


Figure 16.

Semilogarithmic plot of respiratory activity (units) vs. time during a stimulation (STIM.) and decay of potentiation (AFTERDISCHARGE) to show potential error in measurement of its time constant (τ). The true τ of the decay is 50 s. If the τ is measured as the 63% decay from the true starting level of 50 units, it will give the correct value of 50 s (point A). However, some of the total decrease, the loss of the direct effect of the stimulus, is not part of the exponential function. Thus, if the τ is measured as a 63% decay from the end‐stimulation level of 100 units, then an incorrect τ of only 15.3 s (point B) will be calculated.



Figure 17.

Computer‐generated neural inspiratory (phrenic equivalent) activity in a model that incorporates short‐term potentiation (onset τ, 10 s; offset τ, 50 s) and that mimicks constant blood gases and has no other feedback. Control at left, then a 4 min facilitatory stimulus (bar), and then 5 min of recovery. The STP has almost no effect on the pattern after the first 30 s of stimulation and little effect on the recovery after 2 min. (The irregular patterns in the tracing are pixel effects from the computer screen and have no physiological meaning.)



Figure 18.

Computer‐generated ventilation (liters per minute) and arterial, end‐tidal, and medullary PCO2 during rest (VO2 = 0.25 liter/min), 6 min of exercise ( = 1.0 liter/min), and recovery (see text and footnote for details of model). In panel A the model includes the usual short‐term potentiating (STP) mechanism (τ on = 10 s; τ off = 50 s); it yields a typical and normal ventilatory response to exercise. In panel B the STP has been removed, with the result that ventilation at the end of the 6 min of exercise is slightly less than in the model with STP, all PCO2 values are slightly higher, and there are increased oscillations of ventilation after both onset and cessation of exercise.



Figure 19.

Schematic representation of the ventilatory response to static (handgrip) exercise. Asterisks denote the onset and end of the exercise bout.

From Waldrop


Figure 20.

A, Experimental design for reducing the magnitude of central command required to achieve a muscle tension. The drawing shows how vibration is used to activate primary afferents from the contracting muscles, thereby contributing reflex excitation of the motoneurons innervating the muscle. The same amount of force can be generated as was true without the reflex excitation (on the left) but with a reduced central command component. B, Experimental design for increasing the magnitude of central command required to achieve a muscle tension. The drawing shows how vibration is used to activate primary afferents from a muscle (biceps) antagonist to the contracting muscles, thereby contributing reflex inhibition of the motoneurons innervating the contracting muscle. An increased central command component is required in order for the same amount of force to be generated as was true without the reflex inhibition (on the left).

Adapted from Goodwin et al.


Figure 21.

A, Reduction of central command. The blood pressure, heart rate, and ventilatory responses during a normal contraction are shown by the filled circles and continuous lines; the responses when vibration was used to reduce central command are shown by open circles and interrupted lines. B, Augmentation of central command. The blood pressure, heart rate, and ventilatory responses during a normal contraction are shown by the filled circles and continuous lines; the responses when vibration was used to increase central command are shown by open circles and interrupted lines.

Adapted from Goodwin et al.


Figure 22.

Schematic representation of the ventilatory response to static (handgrip) exercise. Asterisks denote the onset and end of the exercise bout.

From Waldrop


Figure 23.

Effect on heart rate and blood pressure responses to static exercise of neuromuscular blockade and of epidural anesthesia. Left, Comparison of each intervention to control at the same absolute force. Right, Comparison at the same relative force.

From Mitchell et al.


Figure 24.

Effect of intended contraction on heart rate and blood pressure in a totally paralyzed subject. Bars indicate the time when contractions were attempted with values for percentage of MVC.

From Gandevia et al.


Figure 25.

Heart rate and blood pressure responses and rating of perceived exertion (r.p.e. units on scale of 6–20) during progressive exercise to maximal. Filled circles represent exercise during the control study and open circles represent maximal effort as the neuromuscular blockade decreased. Values are means ± SEM.

From Galbo et al.


Figure 26.

Muscle sympathetic nerve activity (MSNA) and force. % MVC, percentage of maximal voluntary contraction. A study from one subject before and during partial neuromuscular blockade with curare.

From Victor et al.


Figure 27.

Effect of muscle fatigue on rating of perceived effort (RPE) and peak increase in skin sympathetic nerve activity [Skin SNA (%)] of the same handgrip force (kg). Data are mean ± SEM. Asterisks denote significant differences from previous handgrip contraction (P < 0.05).

From Vissing et al.


Figure 28.

Hemodynamic values at rest and during work rates of 10, 20, and 30 watts (W) performed with one leg and 2 × 20 W performed with two legs. Open circles represent voluntary dynamic exercise, filled triangles represent electrically induced exercise, and filled rectangles represent electrically induced exercise during epidural anesthesia. Values are mean ± SEM. Asterisk denotes differences between voluntary and electrically induced exercise before epidural anesthesia. Double asterisks denote differences between electrically induced exercise with and without epidural anesthesia.

From Strange et al.


Figure 29.

Cardiac output, heart rate, stroke volume, and blood pressure at rest and during one‐legged exercise at two workloads. Upper three panels in normal subjects with no weakness. (A, right leg; Δ, left leg). Lower four panels in subjects with one weak leg (•, normal leg; τ, weak leg). Values are means (± SD).

From Innes et al.


Figure 30.

Effects of static muscular contraction (elicited by ventral root stimulation) upon arterial pressure, heart rate, and the discharge frequency of a posterior hypothalamic neuron of an anesthetized cat. Note that contraction and other mechanical stimulation of the gastrocnemius muscles increased the discharge frequency of this neuron. Baroreceptor stimulation produced by a phenylephrine‐induced increase in arterial pressure had no significant effect upon this neuron. Location of the neuron is indicated by the filled triangle in the line drawing at bottom.

From Waldrop and Stremel


Figure 31.

Computer‐generated ventilatory and PCO2 responses to dynamic exercise. Panel A shows the normal responses with all mechanisms present. In panel B, only the central command component has been deleted. Notice the loss of the initial fast respiratory component but with the peak response differing little from that observed in panel A. The respiratory response is now dependent upon the rising PCO2. Details of the computer model are described in the text.

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Tony G. Waldrop, Frederic L. Eldridge, Gary A. Iwamoto, Jere H. Mitchell. Central Neural Control of Respiration and Circulation During Exercise. Compr Physiol 2011, Supplement 29: Handbook of Physiology, Exercise: Regulation and Integration of Multiple Systems: 333-380. First published in print 1996. doi: 10.1002/cphy.cp120109