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Neural Control of Vascular Function in Skeletal Muscle

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ABSTRACT

The sympathetic nervous system represents a fundamental homeostatic system that exerts considerable control over blood pressure and the distribution of blood flow. This process has been referred to as neurovascular control. Overall, the concept of neurovascular control includes the following elements: efferent postganglionic sympathetic nerve activity, neurotransmitter release, and the end organ response. Each of these elements reflects multiple levels of control that, in turn, affect complex patterns of change in vascular contractile state. Primarily, this review discusses several of these control layers that combine to produce the integrative physiology of reflex vascular control observed in skeletal muscle. Beginning with three reflexes that provide somewhat dissimilar vascular patterns of response despite similar changes in efferent sympathetic nerve activity, namely, the baroreflex, chemoreflex, and muscle metaboreflex, the article discusses the anatomical and physiological bases of postganglionic sympathetic discharge patterns and recruitment, neurotransmitter release and management, and details of regional variations of receptor density and responses within the microvascular bed. Challenges are addressed regarding the fundamentals of measurement and how conclusions from one response or vascular segment should not be used as an indication of neurovascular control as a generalized physiological dogma. Whereas the bulk of the article focuses on the vasoconstrictor function of sympathetic neurovascular integration, attention is also given to the issues of sympathetic vasodilation as well as the impact of chronic changes in sympathetic activation and innervation on vascular health. © 2016 American Physiological Society. Compr Physiol 6:303‐329, 2016.

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Figure 1. Figure 1. Schematic illustrating the many levels of control and variability that exist within the context of sympathetic vasomotor control. Each component and functional element of the neurovascular junction demonstrates features that heighten the complexity of the system. The components include the efferent postganglionic sympathetic nerve, neurovascular junction and vascular smooth muscle (VSM). The types of challenges associated with quantifying a simplistic description of sympathetic neurovascular transduction are outlined above the schema. Details of these issues are discussed in the text. NPY; neuropeptide Y; NE, norepinephrine; ATP, adenosine triphosphate.
Figure 2. Figure 2. Relative changes in forearm (FVR) and total peripheral (TPR) vascular resistance during −45 mmHg lower body negative pressure as a function of corresponding changes in muscle sympathetic nerve activity (MSNA) measured in the peroneal nerve. Data are from seven individuals in a saline trial and six individuals following a diuretic condition. Adapted from (). Note the high variability in vasomotor responses over the large range of changes in MSNA.
Figure 3. Figure 3. Raw tracing of rebreathing (left) and repeated apnea (right) protocols. Both rebreathing and apneas were associated with pressor responses and sympathetic activation. PETCO2; partial pressure of end tidal carbon dioxide. PETO2; partial pressure of end tidal oxygen. MSNA; muscle sympathetic nerve activity. Pressure; oscillatory blood pressure measured by photoplethysmography from the finger. Note that the act of rebreathing between apneas was associated with a period of sympathetic silence, which preceded a fall in blood pressure. Reprinted with permission from ().
Figure 4. Figure 4. Reflex‐specific differences in total peripheral resistance (TPR) in 19 young healthy females. (Top panel) Two minutes (G1 and G2) of isometric handgrip exercise at 40% of maximal voluntary contraction force, and two minutes of postexercise circulatory occlusion (PECO1 and PECO2) to expose the metaboreflex response. (Bottom panel) The change in TPR for the same group of women during nonhypotensive phases of lower body negative pressure (LBNP), 60° head up tilt (HUT), and the handgrip protocol used in top panel. Data are adapted from ().
Figure 5. Figure 5. Anatomical bundling of postganglionic sympathetic C‐fibers in human peroneal (fibular) nerve. View of how tyrosine hydroxylase‐positive axons are bundled and how the distribution of these bundles varies from one fascicle to another in the human peroneal nerve. The arrow refers to a small fascicle without any sympathetic axons. From (), used with permission.
Figure 6. Figure 6. Examples of peroneal nerve sympathetic action potential firing patterns from a representative individual on going from baseline to a maximal apnea as performed by a free diver. The top left panel illustrates the sympathetic recording. The bottom, left panel illustrates the organization of all bursts from smallest to largest, with the largest occurring late in the breath‐hold period. The action potentials are organized based on their size (i.e., clusters) and in which burst they are observed. The data outline the high probability of smaller and medium‐sized action potentials in most bursts whereas the large action potentials arise in the largest bursts which occur with higher probability in the high stress phase of the test. The dashed lines in the left hand panel indicate (from left to right) the burst sizes observed at baseline prior to the breath hold. The panel on the right illustrates the latency of the action potential signal, as a function of action potential size (organized in clusters) as they arrive at the recording electrode, using the appropriate preceding R‐wave of the electrocardiogram as the reference point. The larger action potentials express faster conduction velocities (shorter latency) indicating that they are likely from larger axons rather than movement of the recording electrode. The bar in the lower panel indicates the clusters of action potentials that were not present at baseline. From (), used with permission.
Figure 7. Figure 7. Summary data reflecting the maximal vasoconstrictor responses in the whole leg under baseline conditions as a function of the total amount of muscle sympathetic nerve activity (MSNA) which preceded the change in leg vascular conductance (LVC) by six cardiac cycles. Color indicates the number of bursts in a cluster that preceded the vasoconstriction: Red; a single burst, green; two bursts, yellow; three bursts, blue; four bursts. These data illustrate the direct relationship between total MSNA and whole leg vasoconstriction. From (), used with permission from Wiley.
Figure 8. Figure 8. Responses of individual arterial vessels of a single preparation to paravascular nerve stimulation at 10 Hz (which elicited maximal constriction). Vessel diameters are plotted as a percentage of their baseline internal diameter. The anatomical classification of each vessel is indicated by abbreviations in the figure; TA, terminal arteriole; MA, main artery; 1°, primary arteriole; 2°, secondary arteriole. The figures in brackets refer to the baseline internal diameter. From (), used with permission from Wiley.
Figure 9. Figure 9. Summary schematic illustrating the topographical arrangement of relative innervation and receptor densities, and sensitivity to sympathetic stimulation, in the microvascular bed. See text for details. α1; alpha 1 adrenergic receptor; α2; alpha 2 adrenergic receptor; Y1, neuropeptide Y Y1 receptor; P2X, purinergic vasoconstrictor receptor. 1A‐5A, first through fifth‐order arterioles. Number of asterisks reflects magnitude of effect. Blank boxes indicate lack of information. See text for details which include a description of variations in α2 expression between the mouse and rat in the gluteus muscle.
Figure 10. Figure 10. Summary schematic representing the autoreceptor mechanisms that control neurotransmitter release into the neurovascular cleft, the enzymatic control of neurotransmitter concentration in the neurovascular cleft, and the interactions amongst the postjunctional sympathetic vasoconstrictor receptors on vascular smooth muscle. See text for details. DPPIV; dipeptidyl peptidase IV, APP; amino peptidase (whose role in NPY metabolism is not clear for skeletal muscle vasculature), α1AR; alpha 1 adrenergic receptor; α2AR; alpha 2 adrenergic receptor; Y1, neuropeptide Y1 receptor,Y2; Y2 receptor, ATP; adenosine triphosphate, P2x1, purinergic vasoconstrictor receptor., NPY; neuropeptide Y, NE; norepinephrine. Arrows represent excitatory or potentiating actions. Blunt arrows represent inhibitory actions.
Figure 11. Figure 11. Relationship between workload, forearm blood flow, and vascular conductance during progressive rhythmic handgrip contractions performed by six young healthy individuals.


Figure 1. Schematic illustrating the many levels of control and variability that exist within the context of sympathetic vasomotor control. Each component and functional element of the neurovascular junction demonstrates features that heighten the complexity of the system. The components include the efferent postganglionic sympathetic nerve, neurovascular junction and vascular smooth muscle (VSM). The types of challenges associated with quantifying a simplistic description of sympathetic neurovascular transduction are outlined above the schema. Details of these issues are discussed in the text. NPY; neuropeptide Y; NE, norepinephrine; ATP, adenosine triphosphate.


Figure 2. Relative changes in forearm (FVR) and total peripheral (TPR) vascular resistance during −45 mmHg lower body negative pressure as a function of corresponding changes in muscle sympathetic nerve activity (MSNA) measured in the peroneal nerve. Data are from seven individuals in a saline trial and six individuals following a diuretic condition. Adapted from (). Note the high variability in vasomotor responses over the large range of changes in MSNA.


Figure 3. Raw tracing of rebreathing (left) and repeated apnea (right) protocols. Both rebreathing and apneas were associated with pressor responses and sympathetic activation. PETCO2; partial pressure of end tidal carbon dioxide. PETO2; partial pressure of end tidal oxygen. MSNA; muscle sympathetic nerve activity. Pressure; oscillatory blood pressure measured by photoplethysmography from the finger. Note that the act of rebreathing between apneas was associated with a period of sympathetic silence, which preceded a fall in blood pressure. Reprinted with permission from ().


Figure 4. Reflex‐specific differences in total peripheral resistance (TPR) in 19 young healthy females. (Top panel) Two minutes (G1 and G2) of isometric handgrip exercise at 40% of maximal voluntary contraction force, and two minutes of postexercise circulatory occlusion (PECO1 and PECO2) to expose the metaboreflex response. (Bottom panel) The change in TPR for the same group of women during nonhypotensive phases of lower body negative pressure (LBNP), 60° head up tilt (HUT), and the handgrip protocol used in top panel. Data are adapted from ().


Figure 5. Anatomical bundling of postganglionic sympathetic C‐fibers in human peroneal (fibular) nerve. View of how tyrosine hydroxylase‐positive axons are bundled and how the distribution of these bundles varies from one fascicle to another in the human peroneal nerve. The arrow refers to a small fascicle without any sympathetic axons. From (), used with permission.


Figure 6. Examples of peroneal nerve sympathetic action potential firing patterns from a representative individual on going from baseline to a maximal apnea as performed by a free diver. The top left panel illustrates the sympathetic recording. The bottom, left panel illustrates the organization of all bursts from smallest to largest, with the largest occurring late in the breath‐hold period. The action potentials are organized based on their size (i.e., clusters) and in which burst they are observed. The data outline the high probability of smaller and medium‐sized action potentials in most bursts whereas the large action potentials arise in the largest bursts which occur with higher probability in the high stress phase of the test. The dashed lines in the left hand panel indicate (from left to right) the burst sizes observed at baseline prior to the breath hold. The panel on the right illustrates the latency of the action potential signal, as a function of action potential size (organized in clusters) as they arrive at the recording electrode, using the appropriate preceding R‐wave of the electrocardiogram as the reference point. The larger action potentials express faster conduction velocities (shorter latency) indicating that they are likely from larger axons rather than movement of the recording electrode. The bar in the lower panel indicates the clusters of action potentials that were not present at baseline. From (), used with permission.


Figure 7. Summary data reflecting the maximal vasoconstrictor responses in the whole leg under baseline conditions as a function of the total amount of muscle sympathetic nerve activity (MSNA) which preceded the change in leg vascular conductance (LVC) by six cardiac cycles. Color indicates the number of bursts in a cluster that preceded the vasoconstriction: Red; a single burst, green; two bursts, yellow; three bursts, blue; four bursts. These data illustrate the direct relationship between total MSNA and whole leg vasoconstriction. From (), used with permission from Wiley.


Figure 8. Responses of individual arterial vessels of a single preparation to paravascular nerve stimulation at 10 Hz (which elicited maximal constriction). Vessel diameters are plotted as a percentage of their baseline internal diameter. The anatomical classification of each vessel is indicated by abbreviations in the figure; TA, terminal arteriole; MA, main artery; 1°, primary arteriole; 2°, secondary arteriole. The figures in brackets refer to the baseline internal diameter. From (), used with permission from Wiley.


Figure 9. Summary schematic illustrating the topographical arrangement of relative innervation and receptor densities, and sensitivity to sympathetic stimulation, in the microvascular bed. See text for details. α1; alpha 1 adrenergic receptor; α2; alpha 2 adrenergic receptor; Y1, neuropeptide Y Y1 receptor; P2X, purinergic vasoconstrictor receptor. 1A‐5A, first through fifth‐order arterioles. Number of asterisks reflects magnitude of effect. Blank boxes indicate lack of information. See text for details which include a description of variations in α2 expression between the mouse and rat in the gluteus muscle.


Figure 10. Summary schematic representing the autoreceptor mechanisms that control neurotransmitter release into the neurovascular cleft, the enzymatic control of neurotransmitter concentration in the neurovascular cleft, and the interactions amongst the postjunctional sympathetic vasoconstrictor receptors on vascular smooth muscle. See text for details. DPPIV; dipeptidyl peptidase IV, APP; amino peptidase (whose role in NPY metabolism is not clear for skeletal muscle vasculature), α1AR; alpha 1 adrenergic receptor; α2AR; alpha 2 adrenergic receptor; Y1, neuropeptide Y1 receptor,Y2; Y2 receptor, ATP; adenosine triphosphate, P2x1, purinergic vasoconstrictor receptor., NPY; neuropeptide Y, NE; norepinephrine. Arrows represent excitatory or potentiating actions. Blunt arrows represent inhibitory actions.


Figure 11. Relationship between workload, forearm blood flow, and vascular conductance during progressive rhythmic handgrip contractions performed by six young healthy individuals.
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Further Reading

John T. Shepherd. Circulation to Skeletal Muscle. Compr Physiol 2011, Supplement 8: Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow: 319-370. First published in print 1983. doi: 10.1002/cphy.cp020311

Michael J. Joyner, Jill N. Barnes, Emma C. Hart, B. Gunnar Wallin, Nisha Charkoudian. Neural Control of the Circulation: How Sex and Age Differences Interact in Humans. Compr Physiol 2014, 5: 193-215. doi: 10.1002/cphy.c140005

Nattie E and Li A. Central chemoreceptors: locations and functions. Compr Physiol 2: 221-254, 2012.


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Neural Control of the Circulation: How Sex and Age Differences Interact in Humans
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J. K. Shoemaker, M. B. Badrov, B. K. Al‐Khazraji, D. N. Jackson. Neural Control of Vascular Function in Skeletal Muscle. Compr Physiol 2015, 6: 303-329. doi: 10.1002/cphy.c150004