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Local Regulation of Microvascular Perfusion

Michael J Davis, Michael A Hill, Lih Kuo

10.1002/cphy.cp020406

Source: Supplement 9: Handbook of Physiology, The Cardiovascular System, Microcirculation

Originally published: 2008

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Historical Perspectives
2 Autoregulation
2.1 Blood Flow Regulation
2.2 Capillary Pressure Regulation
3 Mechanisms of Blood Flow Regulation
3.1 Myogenic Mechanism of Blood Flow Regulation
3.2 Signaling Mechanisms Underlying the Myogenic Response
3.3 Metabolic Mechanisms of Blood Flow Regulation
3.4 Interactions Between Local Blood Flow Control Mechanisms
3.5 Interactions Between Microvascular Control Mechanisms
3.6 Converging Pathways for the Interaction of Local Regulatory Mechanisms
4 Glossary of Abbreviations
Figure 1. Figure 1.

Whole‐organ pressure‐flow relationships. Data recalculated from Refs 34,35,36,37,38,1378. Flows are normalized to flow at P = 100 mmHg, except pulmonary data 1378 are normalized to Ppulmonary artery = 21 mmHg. SKM. skeletal muscle.
Figure 2. Figure 2.

(A) Time course of 2A hemodynamic changes in response to Pp reduction; redrawn from Ref. 52 and used by permission; Pp calculated as (digital artery pressure minus box pressure). Flow decreased initially, but returned to control (arrow) within 2–3 min as the arteriole dilated. (B) Regulation of bat wing 1A flow during mild reductions in Pp; redrawn from Ref. 52 and used by permission; mean data calculated from individual points and fit with third‐order polynomial, weighted by standard error and forced through Pp = 90 mmHg.
Figure 3. Figure 3.

(A) Time course of arteriolar dilation in response to 50‐mmHg reduction in box pressure. Plotted from data in Ref. 52. Pp calculated from digital artery pressure minus box pressure. Values represent averages for 8–15 vessels (error bars omitted for clarity). (B) Average steady‐state bat wing arteriolar diameters as a function of perfusion pressure. Error bars and two points for TAs are omitted for clarity. AA, arcuate arteriole; TA, terminal arteriole. Plotted from data in 52.
Figure 4. Figure 4.

(A) Venular diameters during lowered Pp in cat sartorius muscle. Redrawn from Ref. 70; used by permission. (B) Responses of bat wing venules to lowered pressure. Top: in vivo 2V (unpublished); bottom: in vitro IV from Ref. 73; used by permission. IV, first‐order venule; 2V, second‐order venule.
Figure 5. Figure 5.

(A) Steady‐state capillary diameter changes in bat wing capillaries (control D = 7.6 ± 0.4 μm) as a function of box pressure. Replotted from data in Refs 52,53. (B) Capillary diameter changes during aortic occlusion to Pa = 17 mmHg and subsequent phase of reactive hyperemia. Redrawn from Ref. 79.
Figure 6. Figure 6.

Maintenance of relatively stable tissue volume in cat skeletal muscle during reduced Pp 87. (A) Sample recording; (B) summary data. From 87; used by permission.
Figure 7. Figure 7.

(A) PCvenule measurement during reduction in Pp 40. (B) Stability of transvascular fluid flux and PCvenule pressure as a function of Pa. Solid line = normal tone: dotted line = after papaverine (from Ref. 104); used by permission.
Figure 8. Figure 8.

(A) Bat wing Pc as a function of box pressure (Pbox); redrawn from Ref. 52. Solid line is linear regression line of entire data set; line “a” represents perfect regulation; line “b” represents no regulation. Different symbols represent data for individual capillaries. (B) Single Pc recording analysis redrawn from Ref. 54; used by permission. Solid line represents limits of pressure excursion due to regional vasomotion; line “a” represents perfect regulation; line “b” represents no regulation.
Figure 9. Figure 9.

Relative degrees of (A) Pc compensation and (B) flow compensation during Pp changes (from Ref. 104); used by permission. Numbers on graph are calculated open‐loop gains.
Figure 10. Figure 10.

Types of myogenic behavior. (A) pressure‐induced constriction (133]; used by permission (B) Development of basal arteriolar tone at constant pressure 190: used by permission (C) Negative slope of steady‐state, pressure‐diameter curve 128: used by permission (D) Active pressure‐diameter curve with less positive slope than passive curve 1379: used by permission. Filled symbols denote the passive curve. (E) Increased amplitude and frequency of spontaneous contractions with vessel stretch 139; used by permission. (F) Secondary force development (after initial stretch and stress relaxation) in an isometric smooth muscle preparation The response is evident after a 25% stretch but not after a 10% stretch. Modified from 141: used by permisison.
Figure 11. Figure 11.

The wall tension hypothesis for myogenic regulation of vessel radius (from Ref. 30): used by permission.
Figure 12. Figure 12.

Predicted relationships for myogenically active arterioles functioning as a series‐coupled unit, as homogeneously dilating vessels, or as passive vessels. Top panels show predicted diameter responses for the 3 models, bottom panels show predicted microvascular pressure responses. Dotted lines in insets indicate reference lines for perfect pressure regulation. Top panels from [1380); used by permission. Bottom panels modified from 54 and 1380; used by permission.
Figure 13. Figure 13.

(A) Compilation of myogenic index data, redrawn from Ref. 128; used by permission. See 128 for symbol key. (B) Pressure‐diameter relationships of four different branching orders of rat mesenteric arterioles (from Ref. 130); used by permission.
Figure 14. Figure 14.

Schematic diagram illustrating general signaling events underlying the arteriolar myogenic response. An increase in intraluminal pressure provides the initial stimulus through stretch of a smooth muscle membrane or cytoskeletal element or a change in wall tension. Detection of the stimulus occurs either directly at the level of the membrane or as a result of extracellular matrix‐integrin interactions. Subsequent ion channel‐based mechanisms lead to membrane depolarization, increased conductance of voltage‐gated Ca2+ channels, and increased intracellular Ca2+ levels. Ca2+‐ mediated activation of the contractile proteins then initiates contraction. This basic mechanism may also be acted upon by various second messengers to further enhance the level of contraction. Negative feedback mechanisms may also be initiated to limit the extent of contraction thus preventing an unstable feed‐forward system (dotted lines).
Figure 15. Figure 15.

Relationships between membrane potential (Em) and mechanical stimulation. (A) The change in Em for isolated arteriolar smooth muscle cells subjected to defined length increases applied by the movement of glass micropipettes 250; the degree of cell stretch is comparable to that exerted by a modest pressure increase in isolated arterioles. From 250; used by permission. (B) The effect of intraluminal pressure on Em for cannulated cerebral (squares; 280) and cremaster muscle arterioles (triangles. 262; used by permission. Numbers in parentheses indicate pressure in mmHg. (C) Data from panel B plotted as a function of the calculated level of active myogenic tone. From 261; used by permission. Numbers in parenthesis indicate pressure in mmHg. The data suggest a sigmoidal relationship between Em and myogenic tone and suggest differences between vessels from different vascular beds.
Figure 16. Figure 16.

Postulated ion channel mechanisms linking a pressure or stretch stimulus to depolarization and ultimately contraction. Modified from 134; used by permission.
Figure 17. Figure 17.

Involvement of K+ channels in the regulation of myogenic contraction. The figure illustrates two concepts whereby firstly K+ channel inhibition, via generation of the eicosanoid 20‐HETE, leads to depolarization and contraction and secondly by virtue of restricted domains formed by close apposition of the plasma and SR membranes where activation of K+ channels provides a hyperpolarization and relaxation. The two pathways modulate voltage‐gated Ca2+ entry via their effects on Em.
Figure 18. Figure 18.

Relationships between intraluminal pressure, [Ca2+]i, and wall tension for cannulated, fura 2‐loaded, rat cremaster muscle first‐order arterioles. (A) Effect of intraluminal pressure on global smooth muscle [Ca2+]i levels calculated from the 340/380 nm fluorescent ratio (R 340/380). Data shown for active and passive states; n, number of vessels. From 172; used by permission. (B) Relationship between calculated wall tension and [Ca2+]i. A significant (r2 = 0.72, P < 0.001) linear correlation was obtained between tension and [Ca2+]i. From 172; used by permission.
Figure 19. Figure 19.

Connectivity between arteriolar smooth muscle and endothelial cells. (A) Electromicrograph of a rat cremaster first‐order arteriole highlighting junctional connections between endothelial cells and between smooth muscle and endothelial cells. This supports the syncytial nature of the arteriolar wall and the likelihood of gap junctional communication between the two cell types. Modified from 1381; used by permission. (B) Schematic of interactions between smooth muscle and endothelial cells at the biochemical level. Communication is viewed to occur both through gap junctions and the localized release of paracrine factors. McSherry and Dora, personal communication.
Figure 20. Figure 20.

Temporal nature of signaling events following an increase in arteriolar pressure. Multiple pathways are hypothesized to be initiated by the mechanical stimulus, with progression to intermediate and longer term responses being a function of the effectiveness of the initial contractile response. From 1382: used by permission from IOS Press.
Figure 21. Figure 21.

(A) Reactive hyperemia in the dog coronary circulation. CF = coronary flow; RH = reactive hyperemia. From 593; used by permission. (B) Reactive hyperemia in single cat sartorius muscle capillaries. From 592; used by permission.
Figure 22. Figure 22.

Time course of diameter. PO2 and pressure changes during and after local arteriolar occlusion. 1‐min occlusions. Whalen‐style PO2 microelectrodes 602 were used to measure PO2 levels in the tissue (from Ref. 600): used by permission
Figure 23. Figure 23.

(A) Reactive dilation in isolated rat gracilis arterioles (B) Endothelium‐derived NO mediates ∼35% of the reactive dilation 610; used by permission.
Figure 24. Figure 24.

Little effect of superfusate O2 on reactive hyperemia of hamster cheek pouch arterioles (from Ref. [597)); used by permission.
Figure 25. Figure 25.

(A) Capillary velocity and tissue PO2 changes during and after arterial occlusion from Ref. 618; used by permission. (B) Time course of changes in tissue oxidative metabolism (NADH fluorescence; diamonds) and PO2 (circles) in resting rat spinotrapezius after occlusion of feed artery/vein. Modified from Ref. 616; used by permission.
Figure 26. Figure 26.

Proposed contributions of different factors to the various phases of reactive hyperemia 610.
Figure 27. Figure 27.

(A) Functional capillary units in hamster cremaster muscle (from Ref. 967). (B) Changes in indexes of capillary perfusion in hamster cremaster muscle during electrical stimulation of single fibers (from Ref. 680); used by permission.
Figure 28. Figure 28.

(A) Distribution of tissue PO2 measurements made blindly in cat myocardium: modified from Ref. 633; used by permission. Note increase in number of sites with PO2 < 5 mmHg at lower Pp. (B) Change in tissue PO2 during electrical stimulation of the rat spinotrapezius muscle. Open symbols denote points that are significantly different from control value (mean PO2 = 28 mmHg). Suffusate PO2 was ∼14 mmHg From 640; used by permission.
Figure 29. Figure 29.

A) Graded arteriolar dilation as a function of muscle fiber stimulation frequency from Ref. 712; used by permission. (B) Arteriolar dilation precedes fall in tissue PO2 in hamster cheek pouch microcirculation. Modified from Ref. 764; used by permission.
Figure 30. Figure 30.

(A) Longitudinal distribution of perivascular PO2 at various levels of suffusate PO2. Symbols indicate different solution PO2. PCO2 = 32mmHg in all cases. Modified from Ref. [1035); used by permission. (B) Longitudinal distribution of perivascular PO2 in rat cremaster muscle when superfusate PO2 <10 mmHg. Modified from Ref. 631; used by permission.
Figure 31. Figure 31.

(A) Effects of local (micropipette) and global (suffusion) oxygenated solutions on diameter of an aparenchymal cheek pouch arteriole. From 785; used by permission. (B) Summary data for free‐flowing and occluded (no‐flow) aparenchymal arterioles at high and low PO2. Replotted from Ref. 785; used by permission.
Figure 32. Figure 32.

(A) Responses of isolated cerebral arterioles to various concentrations of K+ (B) Responses of same vessels to elevated [K+] in the presence of 50μM Ba2+ to block KIR channels. From Ref. 918: used by permission.
Figure 33. Figure 33.

Effect of extravascular acidosis on coronary arteriolar diameter. (A) Hydrogen ions dilated the coronary arteriole in a concentration‐dependent manner. After replacing with normal pH solution (i.e. washout with pH = 7.4), the diameter returned to the baseline level. (B) Exposure of the vessel to KATP channel inhibitor glibenclamide (5 μM) for 20 min did not alter the baseline diameter of the vessel, but the dilation in response to an increase in hydrogen ion concentration (pH = 7.2) was abolished. Modified from Ref. 1056; used by permission.
Figure 34. Figure 34.

Effect of hyperosmolarity on vascular tone. (A) A coronary arteriole dilated to an increase in extravascular osmolarity by replacing the vessel bath solution containing a high concentration of glucose. Hyperosmolarity produced a sustained arteriolar dilation and vascular tone recovered after washout. (B) Coronary arteriolar dilation to the hyperosmotic glucose solution was inhibited after denudation. (C): Intraluminal KCl (80mM) or KATP channel inhibitor glibenclamide (Glib. 1 μM) significantly attenuated the vasodilation to hyperosmotic glucose. Lumenal diameters were normalized to maximum dilation in response to sodium nitroprusside (0.1 mM). Modified from Ref. 1085; used by permission.
Figure 35. Figure 35.

Segmental coronary microvascular dilation to increased flow (shear stress) at constant mean luminal pressure. Luminal diameters were normalized to resting diameter in the absence of flow. The hierarchy of shear stress‐induced response was large arterioles > intermediate arterioles > small arterioles = small arteries. Modified from Ref. 1186; used by permission.
Figure 36. Figure 36.

Segmental coronary microvascular dilation to adenosine at constant mean luminal pressure without flow. Luminal diameters were normalized to maximum dilation in response to sodium nitroprusside (0.1 mM). The hierarchy of adenosine‐induced response was small arterioles > intermediate arterioles > large arterioles = small arteries. Modified from Ref. 1186; used by permission.
Figure 37. Figure 37.

Scheme for series‐coupled, segmental responsiveness of an arterial network to flow, pressure, metabolic, and adrenergic stimuli. Note that each vasoactive mechanism has a dominant site of action in a particular microvascular segment. All responses are normalized to their maximum. Modified from Ref. 1383; used by permission.
Figure 38. Figure 38.

Integrative regulation of coronary flow by metabolic, myogenic, and shear stress‐induced mechanisms in response to metabolic activation. The sequential, series recruitment of metabolic, myogenic, and flow‐induced dilation in the arteriolar network would optimize functional hyperemia.
Figure 39. Figure 39.

(A) Diagram showing preparation for study of conducted responses using an arteriole from the mouse cremaster muscle in vivo. ACh or KCl is applied locally from a micropipette while observing the arteriolar diameter change either locally or at various remote sites upstream in the flow path. Suffusate flow is in the same direction as blood flow. (B) Arteriolar dilation is observed at the local site of ACh application (time = 0) and the dilation is rapidly conducted to sites 660 and 1320 μm upstream, with partial attenuation of the response. (C) In response to KCl application, arteriolar constriction is observed at the local site and the constriction is conducted upstream, with substantial attenuation at the 660 μm observation site, and complete attenuation of the response 1320 μm away. From Ref. 1261; used by permission.
Figure 40. Figure 40.

Conducted dilation to adenosine in an isolated coronary arteriole (50‐110 μm, ID). Diagram at top shows the experimental set‐up. (A) Adenosine (10 μM) application from a micropipette induces a substantial dilation at the application site that is rapidly conducted upstream to the remote site (>800 μm away). (B) The conducted response but not the local response is blocked by Ba2+ (30μM) in the suffsate. Modified from Ref. 1246; used by permission.
Figure 41. Figure 41.

(A) Segmental resistance changes in cat skeletal muscle in response to transmural pressure elevation using a plethysmograph. Resistances were calculated continuously from total flow and segmental pressures measured by indwelling microcatheters. From 159; used by permission. Vertical lines and A, B labels were added. (B) Constriction of bat wing 2A in response to transmural pressure elevation. Arteriolar pressure increase is sustained, but flow initially increases (dotted line indicates reference flow level), then decreases secondarily modified from Ref. 53; used by permission.
Figure 42. Figure 42.

(A) Arteriolar dilations under free flow and no‐flow conditions; Modified from Ref. 169; used by permission. (B) Arteriolar dilations upstream and downstream from an occlusion. Superfusion solution equilibrated with 0% O2. Modified from Ref. 597; used by permission.
Figure 43. Figure 43.

Interaction between pressure‐induced myogenic responses and flow‐induced vasodilation in isolated subepicardial arterioles. (A) Myogenic constriction (initiated by an increase in intraluminal pressure. (IP) was attenuated in the presence of flow (initiated by a pressure gradient. ΔP, longitudinally across the vessel). (B) Myogenic dilation was enhanced by flow. (C) Flow‐induced dilation was attenuated by elevating IP (D) Flow‐induced dilation was potentiated by lowering IP from Ref. 1174; used by permission.
Figure 44. Figure 44.

(A) Pressure‐diameter relations (myogenic response) of coronary arterioles in the presence and absence of lumenal flow. Myogenic responsiveness was attenuated in the presence of flow. With sodium nitroprusside (10−4M), vessels showed passive responses to intraluminal pressure changes. Lumen diameters were normalized to diameters at intraluminal pressure of 60cmH2O in presence of sodium nitroprusside. Modified from Ref. 1174. (B) How‐induced dilation at different levels of myogenic tone (i.e. 20, 60, and 100cmH2O intraluminal pressure). Intraluminal flow was initiated by increasing pressure gradient longitudinally across the vessel. Lumenal diameters were normalized to passive diameter at respective intraluminal pressure in the presence of sodium nitroprusside (10−4M). Modified from Ref. 1174; used by permission.
Figure 45. Figure 45.

Arteriolar myogenic reactivity during α1‐ and α2‐adrenoceptor constriction. Box‐pressure technique was used to study myogenic responsiveness in first‐order rat cremaster arterioles. Myogenic constriction was insignificant under control conditions (no α tone). In the presence of either type of adrenoceptor tone, myogenic constriction was augmented. With α2 tone, myogenic vasodilation was 3‐ to 4‐fold more pronounced than with α tone. Modified from Ref. 1306; used by permission.


Figure 1.

Whole‐organ pressure‐flow relationships. Data recalculated from Refs 34,35,36,37,38,1378. Flows are normalized to flow at P = 100 mmHg, except pulmonary data 1378 are normalized to Ppulmonary artery = 21 mmHg. SKM. skeletal muscle.



Figure 2.

(A) Time course of 2A hemodynamic changes in response to Pp reduction; redrawn from Ref. 52 and used by permission; Pp calculated as (digital artery pressure minus box pressure). Flow decreased initially, but returned to control (arrow) within 2–3 min as the arteriole dilated. (B) Regulation of bat wing 1A flow during mild reductions in Pp; redrawn from Ref. 52 and used by permission; mean data calculated from individual points and fit with third‐order polynomial, weighted by standard error and forced through Pp = 90 mmHg.



Figure 3.

(A) Time course of arteriolar dilation in response to 50‐mmHg reduction in box pressure. Plotted from data in Ref. 52. Pp calculated from digital artery pressure minus box pressure. Values represent averages for 8–15 vessels (error bars omitted for clarity). (B) Average steady‐state bat wing arteriolar diameters as a function of perfusion pressure. Error bars and two points for TAs are omitted for clarity. AA, arcuate arteriole; TA, terminal arteriole. Plotted from data in 52.



Figure 4.

(A) Venular diameters during lowered Pp in cat sartorius muscle. Redrawn from Ref. 70; used by permission. (B) Responses of bat wing venules to lowered pressure. Top: in vivo 2V (unpublished); bottom: in vitro IV from Ref. 73; used by permission. IV, first‐order venule; 2V, second‐order venule.



Figure 5.

(A) Steady‐state capillary diameter changes in bat wing capillaries (control D = 7.6 ± 0.4 μm) as a function of box pressure. Replotted from data in Refs 52,53. (B) Capillary diameter changes during aortic occlusion to Pa = 17 mmHg and subsequent phase of reactive hyperemia. Redrawn from Ref. 79.



Figure 6.

Maintenance of relatively stable tissue volume in cat skeletal muscle during reduced Pp 87. (A) Sample recording; (B) summary data. From 87; used by permission.



Figure 7.

(A) PCvenule measurement during reduction in Pp 40. (B) Stability of transvascular fluid flux and PCvenule pressure as a function of Pa. Solid line = normal tone: dotted line = after papaverine (from Ref. 104); used by permission.



Figure 8.

(A) Bat wing Pc as a function of box pressure (Pbox); redrawn from Ref. 52. Solid line is linear regression line of entire data set; line “a” represents perfect regulation; line “b” represents no regulation. Different symbols represent data for individual capillaries. (B) Single Pc recording analysis redrawn from Ref. 54; used by permission. Solid line represents limits of pressure excursion due to regional vasomotion; line “a” represents perfect regulation; line “b” represents no regulation.



Figure 9.

Relative degrees of (A) Pc compensation and (B) flow compensation during Pp changes (from Ref. 104); used by permission. Numbers on graph are calculated open‐loop gains.



Figure 10.

Types of myogenic behavior. (A) pressure‐induced constriction (133]; used by permission (B) Development of basal arteriolar tone at constant pressure 190: used by permission (C) Negative slope of steady‐state, pressure‐diameter curve 128: used by permission (D) Active pressure‐diameter curve with less positive slope than passive curve 1379: used by permission. Filled symbols denote the passive curve. (E) Increased amplitude and frequency of spontaneous contractions with vessel stretch 139; used by permission. (F) Secondary force development (after initial stretch and stress relaxation) in an isometric smooth muscle preparation The response is evident after a 25% stretch but not after a 10% stretch. Modified from 141: used by permisison.



Figure 11.

The wall tension hypothesis for myogenic regulation of vessel radius (from Ref. 30): used by permission.



Figure 12.

Predicted relationships for myogenically active arterioles functioning as a series‐coupled unit, as homogeneously dilating vessels, or as passive vessels. Top panels show predicted diameter responses for the 3 models, bottom panels show predicted microvascular pressure responses. Dotted lines in insets indicate reference lines for perfect pressure regulation. Top panels from [1380); used by permission. Bottom panels modified from 54 and 1380; used by permission.



Figure 13.

(A) Compilation of myogenic index data, redrawn from Ref. 128; used by permission. See 128 for symbol key. (B) Pressure‐diameter relationships of four different branching orders of rat mesenteric arterioles (from Ref. 130); used by permission.



Figure 14.

Schematic diagram illustrating general signaling events underlying the arteriolar myogenic response. An increase in intraluminal pressure provides the initial stimulus through stretch of a smooth muscle membrane or cytoskeletal element or a change in wall tension. Detection of the stimulus occurs either directly at the level of the membrane or as a result of extracellular matrix‐integrin interactions. Subsequent ion channel‐based mechanisms lead to membrane depolarization, increased conductance of voltage‐gated Ca2+ channels, and increased intracellular Ca2+ levels. Ca2+‐ mediated activation of the contractile proteins then initiates contraction. This basic mechanism may also be acted upon by various second messengers to further enhance the level of contraction. Negative feedback mechanisms may also be initiated to limit the extent of contraction thus preventing an unstable feed‐forward system (dotted lines).



Figure 15.

Relationships between membrane potential (Em) and mechanical stimulation. (A) The change in Em for isolated arteriolar smooth muscle cells subjected to defined length increases applied by the movement of glass micropipettes 250; the degree of cell stretch is comparable to that exerted by a modest pressure increase in isolated arterioles. From 250; used by permission. (B) The effect of intraluminal pressure on Em for cannulated cerebral (squares; 280) and cremaster muscle arterioles (triangles. 262; used by permission. Numbers in parentheses indicate pressure in mmHg. (C) Data from panel B plotted as a function of the calculated level of active myogenic tone. From 261; used by permission. Numbers in parenthesis indicate pressure in mmHg. The data suggest a sigmoidal relationship between Em and myogenic tone and suggest differences between vessels from different vascular beds.



Figure 16.

Postulated ion channel mechanisms linking a pressure or stretch stimulus to depolarization and ultimately contraction. Modified from 134; used by permission.



Figure 17.

Involvement of K+ channels in the regulation of myogenic contraction. The figure illustrates two concepts whereby firstly K+ channel inhibition, via generation of the eicosanoid 20‐HETE, leads to depolarization and contraction and secondly by virtue of restricted domains formed by close apposition of the plasma and SR membranes where activation of K+ channels provides a hyperpolarization and relaxation. The two pathways modulate voltage‐gated Ca2+ entry via their effects on Em.



Figure 18.

Relationships between intraluminal pressure, [Ca2+]i, and wall tension for cannulated, fura 2‐loaded, rat cremaster muscle first‐order arterioles. (A) Effect of intraluminal pressure on global smooth muscle [Ca2+]i levels calculated from the 340/380 nm fluorescent ratio (R 340/380). Data shown for active and passive states; n, number of vessels. From 172; used by permission. (B) Relationship between calculated wall tension and [Ca2+]i. A significant (r2 = 0.72, P < 0.001) linear correlation was obtained between tension and [Ca2+]i. From 172; used by permission.



Figure 19.

Connectivity between arteriolar smooth muscle and endothelial cells. (A) Electromicrograph of a rat cremaster first‐order arteriole highlighting junctional connections between endothelial cells and between smooth muscle and endothelial cells. This supports the syncytial nature of the arteriolar wall and the likelihood of gap junctional communication between the two cell types. Modified from 1381; used by permission. (B) Schematic of interactions between smooth muscle and endothelial cells at the biochemical level. Communication is viewed to occur both through gap junctions and the localized release of paracrine factors. McSherry and Dora, personal communication.



Figure 20.

Temporal nature of signaling events following an increase in arteriolar pressure. Multiple pathways are hypothesized to be initiated by the mechanical stimulus, with progression to intermediate and longer term responses being a function of the effectiveness of the initial contractile response. From 1382: used by permission from IOS Press.



Figure 21.

(A) Reactive hyperemia in the dog coronary circulation. CF = coronary flow; RH = reactive hyperemia. From 593; used by permission. (B) Reactive hyperemia in single cat sartorius muscle capillaries. From 592; used by permission.



Figure 22.

Time course of diameter. PO2 and pressure changes during and after local arteriolar occlusion. 1‐min occlusions. Whalen‐style PO2 microelectrodes 602 were used to measure PO2 levels in the tissue (from Ref. 600): used by permission



Figure 23.

(A) Reactive dilation in isolated rat gracilis arterioles (B) Endothelium‐derived NO mediates ∼35% of the reactive dilation 610; used by permission.



Figure 24.

Little effect of superfusate O2 on reactive hyperemia of hamster cheek pouch arterioles (from Ref. [597)); used by permission.



Figure 25.

(A) Capillary velocity and tissue PO2 changes during and after arterial occlusion from Ref. 618; used by permission. (B) Time course of changes in tissue oxidative metabolism (NADH fluorescence; diamonds) and PO2 (circles) in resting rat spinotrapezius after occlusion of feed artery/vein. Modified from Ref. 616; used by permission.



Figure 26.

Proposed contributions of different factors to the various phases of reactive hyperemia 610.



Figure 27.

(A) Functional capillary units in hamster cremaster muscle (from Ref. 967). (B) Changes in indexes of capillary perfusion in hamster cremaster muscle during electrical stimulation of single fibers (from Ref. 680); used by permission.



Figure 28.

(A) Distribution of tissue PO2 measurements made blindly in cat myocardium: modified from Ref. 633; used by permission. Note increase in number of sites with PO2 < 5 mmHg at lower Pp. (B) Change in tissue PO2 during electrical stimulation of the rat spinotrapezius muscle. Open symbols denote points that are significantly different from control value (mean PO2 = 28 mmHg). Suffusate PO2 was ∼14 mmHg From 640; used by permission.



Figure 29.

A) Graded arteriolar dilation as a function of muscle fiber stimulation frequency from Ref. 712; used by permission. (B) Arteriolar dilation precedes fall in tissue PO2 in hamster cheek pouch microcirculation. Modified from Ref. 764; used by permission.



Figure 30.

(A) Longitudinal distribution of perivascular PO2 at various levels of suffusate PO2. Symbols indicate different solution PO2. PCO2 = 32mmHg in all cases. Modified from Ref. [1035); used by permission. (B) Longitudinal distribution of perivascular PO2 in rat cremaster muscle when superfusate PO2 <10 mmHg. Modified from Ref. 631; used by permission.



Figure 31.

(A) Effects of local (micropipette) and global (suffusion) oxygenated solutions on diameter of an aparenchymal cheek pouch arteriole. From 785; used by permission. (B) Summary data for free‐flowing and occluded (no‐flow) aparenchymal arterioles at high and low PO2. Replotted from Ref. 785; used by permission.



Figure 32.

(A) Responses of isolated cerebral arterioles to various concentrations of K+ (B) Responses of same vessels to elevated [K+] in the presence of 50μM Ba2+ to block KIR channels. From Ref. 918: used by permission.



Figure 33.

Effect of extravascular acidosis on coronary arteriolar diameter. (A) Hydrogen ions dilated the coronary arteriole in a concentration‐dependent manner. After replacing with normal pH solution (i.e. washout with pH = 7.4), the diameter returned to the baseline level. (B) Exposure of the vessel to KATP channel inhibitor glibenclamide (5 μM) for 20 min did not alter the baseline diameter of the vessel, but the dilation in response to an increase in hydrogen ion concentration (pH = 7.2) was abolished. Modified from Ref. 1056; used by permission.



Figure 34.

Effect of hyperosmolarity on vascular tone. (A) A coronary arteriole dilated to an increase in extravascular osmolarity by replacing the vessel bath solution containing a high concentration of glucose. Hyperosmolarity produced a sustained arteriolar dilation and vascular tone recovered after washout. (B) Coronary arteriolar dilation to the hyperosmotic glucose solution was inhibited after denudation. (C): Intraluminal KCl (80mM) or KATP channel inhibitor glibenclamide (Glib. 1 μM) significantly attenuated the vasodilation to hyperosmotic glucose. Lumenal diameters were normalized to maximum dilation in response to sodium nitroprusside (0.1 mM). Modified from Ref. 1085; used by permission.



Figure 35.

Segmental coronary microvascular dilation to increased flow (shear stress) at constant mean luminal pressure. Luminal diameters were normalized to resting diameter in the absence of flow. The hierarchy of shear stress‐induced response was large arterioles > intermediate arterioles > small arterioles = small arteries. Modified from Ref. 1186; used by permission.



Figure 36.

Segmental coronary microvascular dilation to adenosine at constant mean luminal pressure without flow. Luminal diameters were normalized to maximum dilation in response to sodium nitroprusside (0.1 mM). The hierarchy of adenosine‐induced response was small arterioles > intermediate arterioles > large arterioles = small arteries. Modified from Ref. 1186; used by permission.



Figure 37.

Scheme for series‐coupled, segmental responsiveness of an arterial network to flow, pressure, metabolic, and adrenergic stimuli. Note that each vasoactive mechanism has a dominant site of action in a particular microvascular segment. All responses are normalized to their maximum. Modified from Ref. 1383; used by permission.



Figure 38.

Integrative regulation of coronary flow by metabolic, myogenic, and shear stress‐induced mechanisms in response to metabolic activation. The sequential, series recruitment of metabolic, myogenic, and flow‐induced dilation in the arteriolar network would optimize functional hyperemia.



Figure 39.

(A) Diagram showing preparation for study of conducted responses using an arteriole from the mouse cremaster muscle in vivo. ACh or KCl is applied locally from a micropipette while observing the arteriolar diameter change either locally or at various remote sites upstream in the flow path. Suffusate flow is in the same direction as blood flow. (B) Arteriolar dilation is observed at the local site of ACh application (time = 0) and the dilation is rapidly conducted to sites 660 and 1320 μm upstream, with partial attenuation of the response. (C) In response to KCl application, arteriolar constriction is observed at the local site and the constriction is conducted upstream, with substantial attenuation at the 660 μm observation site, and complete attenuation of the response 1320 μm away. From Ref. 1261; used by permission.



Figure 40.

Conducted dilation to adenosine in an isolated coronary arteriole (50‐110 μm, ID). Diagram at top shows the experimental set‐up. (A) Adenosine (10 μM) application from a micropipette induces a substantial dilation at the application site that is rapidly conducted upstream to the remote site (>800 μm away). (B) The conducted response but not the local response is blocked by Ba2+ (30μM) in the suffsate. Modified from Ref. 1246; used by permission.



Figure 41.

(A) Segmental resistance changes in cat skeletal muscle in response to transmural pressure elevation using a plethysmograph. Resistances were calculated continuously from total flow and segmental pressures measured by indwelling microcatheters. From 159; used by permission. Vertical lines and A, B labels were added. (B) Constriction of bat wing 2A in response to transmural pressure elevation. Arteriolar pressure increase is sustained, but flow initially increases (dotted line indicates reference flow level), then decreases secondarily modified from Ref. 53; used by permission.



Figure 42.

(A) Arteriolar dilations under free flow and no‐flow conditions; Modified from Ref. 169; used by permission. (B) Arteriolar dilations upstream and downstream from an occlusion. Superfusion solution equilibrated with 0% O2. Modified from Ref. 597; used by permission.



Figure 43.

Interaction between pressure‐induced myogenic responses and flow‐induced vasodilation in isolated subepicardial arterioles. (A) Myogenic constriction (initiated by an increase in intraluminal pressure. (IP) was attenuated in the presence of flow (initiated by a pressure gradient. ΔP, longitudinally across the vessel). (B) Myogenic dilation was enhanced by flow. (C) Flow‐induced dilation was attenuated by elevating IP (D) Flow‐induced dilation was potentiated by lowering IP from Ref. 1174; used by permission.



Figure 44.

(A) Pressure‐diameter relations (myogenic response) of coronary arterioles in the presence and absence of lumenal flow. Myogenic responsiveness was attenuated in the presence of flow. With sodium nitroprusside (10−4M), vessels showed passive responses to intraluminal pressure changes. Lumen diameters were normalized to diameters at intraluminal pressure of 60cmH2O in presence of sodium nitroprusside. Modified from Ref. 1174. (B) How‐induced dilation at different levels of myogenic tone (i.e. 20, 60, and 100cmH2O intraluminal pressure). Intraluminal flow was initiated by increasing pressure gradient longitudinally across the vessel. Lumenal diameters were normalized to passive diameter at respective intraluminal pressure in the presence of sodium nitroprusside (10−4M). Modified from Ref. 1174; used by permission.



Figure 45.

Arteriolar myogenic reactivity during α1‐ and α2‐adrenoceptor constriction. Box‐pressure technique was used to study myogenic responsiveness in first‐order rat cremaster arterioles. Myogenic constriction was insignificant under control conditions (no α tone). In the presence of either type of adrenoceptor tone, myogenic constriction was augmented. With α2 tone, myogenic vasodilation was 3‐ to 4‐fold more pronounced than with α tone. Modified from Ref. 1306; used by permission.

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Article Title: Local Regulation of Microvascular Perfusion
 

How to Cite

Michael J Davis, Michael A Hill, Lih Kuo. Local Regulation of Microvascular Perfusion. Compr Physiol 2011, Supplement 9: Handbook of Physiology, The Cardiovascular System, Microcirculation: 161-284. First published in print 2008. doi: 10.1002/cphy.cp020406