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Autonomic Adjustments to Exercise in Humans

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ABSTRACT

Autonomic nervous system adjustments to the heart and blood vessels are necessary for mediating the cardiovascular responses required to meet the metabolic demands of working skeletal muscle during exercise. These demands are met by precise exercise intensity‐dependent alterations in sympathetic and parasympathetic nerve activity. The purpose of this review is to examine the contributions of the sympathetic and parasympathetic nervous systems in mediating specific cardiovascular and hemodynamic responses to exercise. These changes in autonomic outflow are regulated by several neural mechanisms working in concert, including central command (a feed forward mechanism originating from higher brain centers), the exercise pressor reflex (a feed‐back mechanism originating from skeletal muscle), the arterial baroreflex (a negative feed‐back mechanism originating from the carotid sinus and aortic arch), and cardiopulmonary baroreceptors (a feed‐back mechanism from stretch receptors located in the heart and lungs). In addition, arterial chemoreceptors and phrenic afferents from respiratory muscles (i.e., respiratory metaboreflex) are also capable of modulating the autonomic responses to exercise. Our goal is to provide a detailed review of the parasympathetic and sympathetic changes that occur with exercise distinguishing between the onset of exercise and steady‐state conditions, when appropriate. In addition, studies demonstrating the contributions of each of the aforementioned neural mechanisms to the autonomic changes and ensuing cardiac and/or vascular responses will be covered. © 2015 American Physiological Society. Compr Physiol 5:475‐512, 2015.

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Figure 1. Figure 1. Schematic summarizing the mechanisms involved in mediating the autonomic adjustments to exercise. Neural signals originating from higher brain centers (i.e., central command), chemically sensitive receptors in the carotid and aortic bodies (i.e., arterial chemoreflex), stretch receptors in the carotid and aortic arteries (i.e., arterial baroreflex), mechanically and metabolically sensitive afferents from skeletal muscle (i.e., exercise pressor reflex), mechanically sensitive stretch receptors in the cardiopulmonary region (i.e., cardiopulmonary baroreflex) and metabolically sensitive afferents from respiratory muscles (i.e., respiratory metaboreflex) are processed within brain cardiovascular control areas that influence efferent sympathetic and parasympathetic nerve activity. The alterations in autonomic outflow elicited by these inputs during exercise evoke changes in cardiac and vascular function, as well as release of catecholamines from the adrenal medulla.
Figure 2. Figure 2. Simplified schematic illustrating putative neural areas involved in the control of parasympathetic and sympathetic outflow. The activity of efferent autonomic outflow is determined by complex interactions within and between central neural circuits, peripheral afferent inputs to the nucleus tractus solitarii (NTS) and other neural areas (not shown) as well as circulating factors. The integrated response of all of these ascending and descending neural signals ultimately determines parasympathetic and sympathetic outflow. See text for additional details. CVLM, caudal ventrolateral medulla; CVO, circumventricular organs; IML, intermediolateral cell column; NA, nucleus ambiguus; RVLM, rostral ventrolateral medulla.
Figure 3. Figure 3. Summary of methods used for measuring regional SNA in humans. Sympathetic nerve firing can be measured directly in postganglionic sympathetic nerve fibers of skin and skeletal muscle using the technique of microneurography. Isotope dilution methods can be used to measure the spillover rates of norepinephrine to plasma from individual organs, which provides an assessment of regional SNA in the limbs as well as specific organs. Cardiac sympathetic nerve scans can be used to study the anatomy of the sympathetic innervation of the heart. Reprinted, with permission, from ().
Figure 4. Figure 4. Muscle SNA, mean arterial pressure (MAP), and HR responses to isometric handgrip (35% MVC) followed by a period of post exercise ischemia (PEI) to isolate the muscle metaboreflex. As originally reported by Mark et al. () HR increases from the onset of exercise, MAP rises more gradually and a delay is present for muscle SNA consistent with muscle metaboreflex mediation. This is supported by the maintenance of muscle SNA and MAP during PEI, a period in which muscle metaboreflex mediated responses are isolated from central command and muscle mechanoreceptors. In contrast, HR returns to baseline values during PEI.
Figure 5. Figure 5. Muscle SNA responses to a bout of incremental leg cycling ranging in intensity from very mild to exhausting. Raw recordings of arterial BP and muscle SNA (MSNA) during rest, very mild, mild, moderate, heavy, and exhausting exercise and recovery in a representative subject from Ichinose et al. (). After an initial decrease in MSNA from rest during very mild exercise, MSNA was increased progressively as exercise intensity increased. Reprinted, with permission, from ().
Figure 6. Figure 6. Imagined and actual handgrip exercise elicits similar cardiovascular responses. Heart rate, mean arterial blood pressure, and rating of perceived exertion during actual (left) and imagined (right) handgrip exercise. Subjects were categorized into low (n = 4) and high (n = 5) hypnotizability groups. Muscle electromyographic recordings demonstrated no measurable increases in force during imagined handgrip, not shown. The data are presented as mean ± SD. *P < 0.05 low versus high hypnotizability. Reprinted, with permission, from ().
Figure 7. Figure 7. Electrophysiology recordings from the periaqueductal gray suggest that this neural region is involved in mediating the cardiovascular adjustments to exercise. Three patients had stimulation electrodes placed in the periaqueductal gray for the treatment of chronic neuropathic pain. Local field potentials (LFP) were collected from the periaqueductal gray during resting conditions, anticipation of exercise, cycling at 15 W (30‐60 s) and recovery from exercise. (A) Original LFP recordings from the periaqueductal gray. (B) Magnetic resonance image illustrating electrode placement in the periaqueductal gray. (C) Mean power spectral density from all three subjects. (D) Normalized spectral changes (rest = 1.0) divided into frequency bands. *P < 0.05, **P < 0.01, ***P < 0.001 versus rest. Reprinted, with permission, from ().
Figure 8. Figure 8. Augmenting the level of central command with partial neuromuscular blockade exaggerates the cardiovascular responses to static handgrip exercise. Mean arterial blood pressure and heart rate at rest, during a 2 min handgrip contraction at 15% maximal voluntary contraction (dashed lines) and for 2 min of recovery. The data are presented as the mean from 12 healthy subjects (5 female). • control, ○ contraction with tubocurarine that the subjects were able to maintain for 2 min, □ contraction with tubocurarine that the subjects were not able to maintain throughout the 2 min exercise period. ▴ P < 0.05 resting and exercise values during tubocurarine are different from control. Reprinted, with permission, from ().
Figure 9. Figure 9. Original report identifying a BP‐raising reflex originating in skeletal muscle in humans. (A) Schematic showing preparation for the experimental protocol used in which a cuff was placed around the exercising forearm to perform ischemic exercise, while a cuff on the opposite arm was used to measure arterial BP. (B) Shows part of the seminal results from this study documenting the mild increase in BP during freely perfused rhythmic exercise (top panel) in comparison to the massive increase in systolic BP during and after exercise when the forearm was made ischemic by cuff inflation to supra‐systolic pressure. Reprinted, with permission, from ().
Figure 10. Figure 10. Change in R‐R interval evoked by passive calf stretch under control conditions (black bars) and with glycopyrrolate (gray bars). The shortening of the mean (+SE) R‐R interval in response to stretch was significantly (*P < 0.05) attenuated with cholinergic (muscarinic) blockade with glycopyrrolate in 3 subjects. Reprinted, with permission, from ().
Figure 11. Figure 11. Activation of group III and IV skeletal muscle afferents during dynamic exercise induced by stimulation of the mesencephalic locomotor region in cats. Cumulative histograms for 24 group III afferents (A) and 10 group IV afferents (B) before, during, and after dynamic exercise. The exercise period is denoted by horizontal bars. These findings demonstrate that low‐intensity dynamic exercise stimulated both Group III and IV skeletal muscle afferents. Imp, impulses. Reprinted, with permission, from ().
Figure 12. Figure 12. HR responses to isometric handgrip (IHG) and postexercise ischemia (PEI) under control conditions (black symbols), and following β‐adrenergic blockade (light gray symbols) and parasympathetic blockade (dark gray symbols). HR during all experimental phases (A) and change (Δ) in HR from rest (B) are shown. PEI‐M, PEI following 25% IHG; PEI‐H, PEI following 40% IHG. *P < 0.05 versus exercise, †P < 0.05 versus control, ‡P < 0.05 versus β blockade, #P < 0.05 versus 25% MVC. Reprinted, with permission, from ().
Figure 13. Figure 13. Sympathoexcitatory responses to fatiguing static handgrip at 30% MVC in patients with McArdle's disease, who cannot produce lactic acid due to a myophosphorylase deficiency, and age, sex, and bodyweight matched controls. (A) Original muscle SNA (MSNA) record from a patient with McArdle's disease and a control subject with a similar time to fatigue. (B) Summary data showing MSNA, mean arterial pressure (MAP) and HR responses during fatiguing handgrip followed by postexercise forearm ischemia and recovery. The MSNA response to exercise was severely blunted in the McArdle's patients compared to controls. *P < 0.05 versus controls. Reprinted, with permission, from ().
Figure 14. Figure 14. Schematic illustration depicting the afferent and efferent neural responses of the arterial baroreceptors. Reductions in BP in the carotid sinus and aortic arch are sensed by the baroreceptors eliciting decreases in afferent nerve firing. This reduction in neural input to the brainstem causes an increase in sympathetic neural outflow to the heart and vasculature, while at the same time decreasing parasympathetic nerve activity to the heart. Collectively, these reflex‐mediated adjustments are designed to correct the decrease in pressure sensed by the baroreceptors and bring BP back to its original value. The converse occurs when the baroreceptors are exposed to an increase in BP. Adapted, with permission, from ().
Figure 15. Figure 15. Anticipation of exercise blunts carotid baroreflex mediated HR responses. Summary data showing the HR responses to neck suction (NS) at −60 Torr performed at rest and in anticipation of isometric handgrip exercise during four repeat trials. This anticipatory period was used to isolate feedforward central command input in the absence of any feedback from skeletal muscle. To create an anticipatory period, subjects were instructed that immediately after the cessation of NS they must take hold of the handgrip dynamometer and start exercising as rapidly as possible at 45% MVC and sustain the contraction for 1 min. Although a clear blunting of carotid‐cardiac responses was observed in the first two trails, a habituation in the response was found. * represents P < 0.05 versus rest. Unpublished observations made by the authors.
Figure 16. Figure 16. A schematic summary of carotid baroreflex resetting that occurs from rest to heavy exercise. In general, the carotid baroreflex function curve for HR, muscle SNA, and MAP is progressively reset from rest to heavy exercise. However, the functional characteristics of the stimulus‐response curve differ depending on the dependent variable studied. See text for details.
Figure 17. Figure 17. Progressive resetting of the arterial baroreflex control of muscle SNA (MSNA) in the transition from rest to steady‐state two arm cycling exercise. (A) Summary data showing the average operating points (•) with the corresponding mean linear regression lines relating MSNA burst incidence and diastolic BP at rest, unloaded exercise (EX), initial 50% EX, and later 50% EX. (B) Group summary data for the slopes of the linear regression lines between MSNA burst incidence and diastolic BP (i.e., arterial baroreflex sensitivity). These findings indicate that baroreflex control of MSNA is well maintained throughout dynamic exercise in humans, progressively being reset to operate around the exercise‐induced elevations in BP without any changes in reflex sensitivity. See text for further details. Reprinted, with permission, from ().
Figure 18. Figure 18. Original records showing muscle SNA (MSNA; radial nerve) and BP at baseline (control) and during the preparation and initiation of leg cycling exercise at 33 W (panel A) and 166 W (panel B). A notable reduction in MSNA is evident during the preparation and initial stages of exercise at both workloads. Reprinted, with permission, from ().
Figure 19. Figure 19. Transient inhibition of the carotid chemoreflex with inhaled hyperoxia increases exercising leg blood flow and vascular conductance. End‐tidal O2 (PET,O2), femoral artery blood flow and femoral vascular conductance during transient inhaled hyperoxia at rest (left) and during two‐legged knee extension exercise (right). *P < 0.05 versus baseline. Reprinted, with permission, from ().
Figure 20. Figure 20. Summary of the neural control mechanisms underlying the HR response to the onset of exercise, steady‐state exercise, and recovery from exercise. The contribution of changes in cardiac parasympathetic and sympathetic activity and the influence of central command and feedback from metabolically (muscle metaboreceptors) and mechanically (muscle tetanoreceptors) sensitive skeletal muscle afferents are indicated. Reprinted, with permission, from ().


Figure 1. Schematic summarizing the mechanisms involved in mediating the autonomic adjustments to exercise. Neural signals originating from higher brain centers (i.e., central command), chemically sensitive receptors in the carotid and aortic bodies (i.e., arterial chemoreflex), stretch receptors in the carotid and aortic arteries (i.e., arterial baroreflex), mechanically and metabolically sensitive afferents from skeletal muscle (i.e., exercise pressor reflex), mechanically sensitive stretch receptors in the cardiopulmonary region (i.e., cardiopulmonary baroreflex) and metabolically sensitive afferents from respiratory muscles (i.e., respiratory metaboreflex) are processed within brain cardiovascular control areas that influence efferent sympathetic and parasympathetic nerve activity. The alterations in autonomic outflow elicited by these inputs during exercise evoke changes in cardiac and vascular function, as well as release of catecholamines from the adrenal medulla.


Figure 2. Simplified schematic illustrating putative neural areas involved in the control of parasympathetic and sympathetic outflow. The activity of efferent autonomic outflow is determined by complex interactions within and between central neural circuits, peripheral afferent inputs to the nucleus tractus solitarii (NTS) and other neural areas (not shown) as well as circulating factors. The integrated response of all of these ascending and descending neural signals ultimately determines parasympathetic and sympathetic outflow. See text for additional details. CVLM, caudal ventrolateral medulla; CVO, circumventricular organs; IML, intermediolateral cell column; NA, nucleus ambiguus; RVLM, rostral ventrolateral medulla.


Figure 3. Summary of methods used for measuring regional SNA in humans. Sympathetic nerve firing can be measured directly in postganglionic sympathetic nerve fibers of skin and skeletal muscle using the technique of microneurography. Isotope dilution methods can be used to measure the spillover rates of norepinephrine to plasma from individual organs, which provides an assessment of regional SNA in the limbs as well as specific organs. Cardiac sympathetic nerve scans can be used to study the anatomy of the sympathetic innervation of the heart. Reprinted, with permission, from ().


Figure 4. Muscle SNA, mean arterial pressure (MAP), and HR responses to isometric handgrip (35% MVC) followed by a period of post exercise ischemia (PEI) to isolate the muscle metaboreflex. As originally reported by Mark et al. () HR increases from the onset of exercise, MAP rises more gradually and a delay is present for muscle SNA consistent with muscle metaboreflex mediation. This is supported by the maintenance of muscle SNA and MAP during PEI, a period in which muscle metaboreflex mediated responses are isolated from central command and muscle mechanoreceptors. In contrast, HR returns to baseline values during PEI.


Figure 5. Muscle SNA responses to a bout of incremental leg cycling ranging in intensity from very mild to exhausting. Raw recordings of arterial BP and muscle SNA (MSNA) during rest, very mild, mild, moderate, heavy, and exhausting exercise and recovery in a representative subject from Ichinose et al. (). After an initial decrease in MSNA from rest during very mild exercise, MSNA was increased progressively as exercise intensity increased. Reprinted, with permission, from ().


Figure 6. Imagined and actual handgrip exercise elicits similar cardiovascular responses. Heart rate, mean arterial blood pressure, and rating of perceived exertion during actual (left) and imagined (right) handgrip exercise. Subjects were categorized into low (n = 4) and high (n = 5) hypnotizability groups. Muscle electromyographic recordings demonstrated no measurable increases in force during imagined handgrip, not shown. The data are presented as mean ± SD. *P < 0.05 low versus high hypnotizability. Reprinted, with permission, from ().


Figure 7. Electrophysiology recordings from the periaqueductal gray suggest that this neural region is involved in mediating the cardiovascular adjustments to exercise. Three patients had stimulation electrodes placed in the periaqueductal gray for the treatment of chronic neuropathic pain. Local field potentials (LFP) were collected from the periaqueductal gray during resting conditions, anticipation of exercise, cycling at 15 W (30‐60 s) and recovery from exercise. (A) Original LFP recordings from the periaqueductal gray. (B) Magnetic resonance image illustrating electrode placement in the periaqueductal gray. (C) Mean power spectral density from all three subjects. (D) Normalized spectral changes (rest = 1.0) divided into frequency bands. *P < 0.05, **P < 0.01, ***P < 0.001 versus rest. Reprinted, with permission, from ().


Figure 8. Augmenting the level of central command with partial neuromuscular blockade exaggerates the cardiovascular responses to static handgrip exercise. Mean arterial blood pressure and heart rate at rest, during a 2 min handgrip contraction at 15% maximal voluntary contraction (dashed lines) and for 2 min of recovery. The data are presented as the mean from 12 healthy subjects (5 female). • control, ○ contraction with tubocurarine that the subjects were able to maintain for 2 min, □ contraction with tubocurarine that the subjects were not able to maintain throughout the 2 min exercise period. ▴ P < 0.05 resting and exercise values during tubocurarine are different from control. Reprinted, with permission, from ().


Figure 9. Original report identifying a BP‐raising reflex originating in skeletal muscle in humans. (A) Schematic showing preparation for the experimental protocol used in which a cuff was placed around the exercising forearm to perform ischemic exercise, while a cuff on the opposite arm was used to measure arterial BP. (B) Shows part of the seminal results from this study documenting the mild increase in BP during freely perfused rhythmic exercise (top panel) in comparison to the massive increase in systolic BP during and after exercise when the forearm was made ischemic by cuff inflation to supra‐systolic pressure. Reprinted, with permission, from ().


Figure 10. Change in R‐R interval evoked by passive calf stretch under control conditions (black bars) and with glycopyrrolate (gray bars). The shortening of the mean (+SE) R‐R interval in response to stretch was significantly (*P < 0.05) attenuated with cholinergic (muscarinic) blockade with glycopyrrolate in 3 subjects. Reprinted, with permission, from ().


Figure 11. Activation of group III and IV skeletal muscle afferents during dynamic exercise induced by stimulation of the mesencephalic locomotor region in cats. Cumulative histograms for 24 group III afferents (A) and 10 group IV afferents (B) before, during, and after dynamic exercise. The exercise period is denoted by horizontal bars. These findings demonstrate that low‐intensity dynamic exercise stimulated both Group III and IV skeletal muscle afferents. Imp, impulses. Reprinted, with permission, from ().


Figure 12. HR responses to isometric handgrip (IHG) and postexercise ischemia (PEI) under control conditions (black symbols), and following β‐adrenergic blockade (light gray symbols) and parasympathetic blockade (dark gray symbols). HR during all experimental phases (A) and change (Δ) in HR from rest (B) are shown. PEI‐M, PEI following 25% IHG; PEI‐H, PEI following 40% IHG. *P < 0.05 versus exercise, †P < 0.05 versus control, ‡P < 0.05 versus β blockade, #P < 0.05 versus 25% MVC. Reprinted, with permission, from ().


Figure 13. Sympathoexcitatory responses to fatiguing static handgrip at 30% MVC in patients with McArdle's disease, who cannot produce lactic acid due to a myophosphorylase deficiency, and age, sex, and bodyweight matched controls. (A) Original muscle SNA (MSNA) record from a patient with McArdle's disease and a control subject with a similar time to fatigue. (B) Summary data showing MSNA, mean arterial pressure (MAP) and HR responses during fatiguing handgrip followed by postexercise forearm ischemia and recovery. The MSNA response to exercise was severely blunted in the McArdle's patients compared to controls. *P < 0.05 versus controls. Reprinted, with permission, from ().


Figure 14. Schematic illustration depicting the afferent and efferent neural responses of the arterial baroreceptors. Reductions in BP in the carotid sinus and aortic arch are sensed by the baroreceptors eliciting decreases in afferent nerve firing. This reduction in neural input to the brainstem causes an increase in sympathetic neural outflow to the heart and vasculature, while at the same time decreasing parasympathetic nerve activity to the heart. Collectively, these reflex‐mediated adjustments are designed to correct the decrease in pressure sensed by the baroreceptors and bring BP back to its original value. The converse occurs when the baroreceptors are exposed to an increase in BP. Adapted, with permission, from ().


Figure 15. Anticipation of exercise blunts carotid baroreflex mediated HR responses. Summary data showing the HR responses to neck suction (NS) at −60 Torr performed at rest and in anticipation of isometric handgrip exercise during four repeat trials. This anticipatory period was used to isolate feedforward central command input in the absence of any feedback from skeletal muscle. To create an anticipatory period, subjects were instructed that immediately after the cessation of NS they must take hold of the handgrip dynamometer and start exercising as rapidly as possible at 45% MVC and sustain the contraction for 1 min. Although a clear blunting of carotid‐cardiac responses was observed in the first two trails, a habituation in the response was found. * represents P < 0.05 versus rest. Unpublished observations made by the authors.


Figure 16. A schematic summary of carotid baroreflex resetting that occurs from rest to heavy exercise. In general, the carotid baroreflex function curve for HR, muscle SNA, and MAP is progressively reset from rest to heavy exercise. However, the functional characteristics of the stimulus‐response curve differ depending on the dependent variable studied. See text for details.


Figure 17. Progressive resetting of the arterial baroreflex control of muscle SNA (MSNA) in the transition from rest to steady‐state two arm cycling exercise. (A) Summary data showing the average operating points (•) with the corresponding mean linear regression lines relating MSNA burst incidence and diastolic BP at rest, unloaded exercise (EX), initial 50% EX, and later 50% EX. (B) Group summary data for the slopes of the linear regression lines between MSNA burst incidence and diastolic BP (i.e., arterial baroreflex sensitivity). These findings indicate that baroreflex control of MSNA is well maintained throughout dynamic exercise in humans, progressively being reset to operate around the exercise‐induced elevations in BP without any changes in reflex sensitivity. See text for further details. Reprinted, with permission, from ().


Figure 18. Original records showing muscle SNA (MSNA; radial nerve) and BP at baseline (control) and during the preparation and initiation of leg cycling exercise at 33 W (panel A) and 166 W (panel B). A notable reduction in MSNA is evident during the preparation and initial stages of exercise at both workloads. Reprinted, with permission, from ().


Figure 19. Transient inhibition of the carotid chemoreflex with inhaled hyperoxia increases exercising leg blood flow and vascular conductance. End‐tidal O2 (PET,O2), femoral artery blood flow and femoral vascular conductance during transient inhaled hyperoxia at rest (left) and during two‐legged knee extension exercise (right). *P < 0.05 versus baseline. Reprinted, with permission, from ().


Figure 20. Summary of the neural control mechanisms underlying the HR response to the onset of exercise, steady‐state exercise, and recovery from exercise. The contribution of changes in cardiac parasympathetic and sympathetic activity and the influence of central command and feedback from metabolically (muscle metaboreceptors) and mechanically (muscle tetanoreceptors) sensitive skeletal muscle afferents are indicated. Reprinted, with permission, from ().
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James P. Fisher, Colin N. Young, Paul J. Fadel. Autonomic Adjustments to Exercise in Humans. Compr Physiol 2015, 5: 475-512. doi: 10.1002/cphy.c140022