Information Transfer in Microvascular Networks

The adequate and efficient functioning of the circulatory system requires coordination of vessel diameters and of vascular responses to local and remote stimuli. Such coordination implies transfer of information about functional status and demands to all parts of the vascular system. In the peripheral circulation, blood flow must be controlled locally to accommodate spatial variations in demand. This requires information transfer from peripheral vessels to the more proximal vessels that feed and drain them. Principal mechanisms available for this information transfer are hemodynamic coupling, diffusive and convective transport of metabolites, and responses conducted along vessel walls. Current knowledge of these mechanisms is reviewed here. Theoretical models provide a framework for examining how information transfer mechanisms and vascular responses are integrated, so as to provide short‐term regulation of blood flow and long‐term structural adaptation of microvascular networks.

[1]  T. Skalak,et al.  The Role of Mechanical Stresses in Microvascular Remodeling , 1996, Microcirculation.

[2]  I. Sarelius,et al.  Role For Capillaries In Coupling Blood Flow With Metabolism , 2000, Clinical and experimental pharmacology & physiology.

[3]  K. Tyml,et al.  Comparable effects of arteriolar and capillary stimuli on blood flow in rat skeletal muscle. , 1997, Microvascular research.

[4]  R G Dacey,et al.  Local and conducted vasomotor responses in isolated rat cerebral arterioles. , 1996, The American journal of physiology.

[5]  R. Berne,et al.  Propagated Vasodilation in the Microcirculation of the Hamster Cheek Pouch , 1970, Circulation research.

[6]  Y. Ouellette,et al.  Evidence for K+ channels involvement in capillary sensing and for bidirectionality in capillary communication. , 1997, Microvascular research.

[7]  R. Hester,et al.  Venular-arteriolar diffusion of adenosine in hamster cremaster microcirculation. , 1990, The American journal of physiology.

[8]  K. Tyml,et al.  Evidence for sensing and integration of biological signals by the capillary network. , 1993, The American journal of physiology.

[9]  M Ursino,et al.  Vasomotion and blood flow regulation in hamster skeletal muscle microcirculation: A theoretical and experimental study. , 1998, Microvascular research.

[10]  B L Langille,et al.  Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. , 1986, Science.

[11]  M. J. Davis,et al.  Signaling mechanisms underlying the vascular myogenic response. , 1999, Physiological reviews.

[12]  J. Beach,et al.  Capillaries and arterioles are electrically coupled in hamster cheek pouch. , 1998, American journal of physiology. Heart and circulatory physiology.

[13]  W. Jackson,et al.  Arteriolar oxygen reactivity: where is the sensor? , 1987, The American journal of physiology.

[14]  R. Rivers Cumulative conducted vasodilation within a single arteriole and the maximum conducted response. , 1997, The American journal of physiology.

[15]  J. Faber,et al.  Inhibition of arteriole alpha 2- but not alpha 1-adrenoceptor constriction by acidosis and hypoxia in vitro. , 1995, The American journal of physiology.

[16]  A. Pries,et al.  Structure and hemodynamics of microvascular networks: heterogeneity and correlations. , 1995, The American journal of physiology.

[17]  S. Segal,et al.  Effect of motor unit recruitment on functional vasodilatation in hamster retractor muscle , 2000, The Journal of physiology.

[18]  J. Spaan,et al.  Shear stress is not sufficient to control growth of vascular networks: a model study. , 1996, The American journal of physiology.

[19]  B. Reglin,et al.  Structural adaptation of microvascular networks: functional roles of adaptive responses. , 2001, American journal of physiology. Heart and circulatory physiology.

[20]  K. Aukland,et al.  A Mathematical Analysis of the Myogenic Hypothesis with Special Reference to Autoregulation of Renal Blood Flow , 1983, Circulation research.

[21]  Donald G Welsh,et al.  Endothelial and smooth muscle cell conduction in arterioles controlling blood flow. , 1998, American journal of physiology. Heart and circulatory physiology.

[22]  J. Faber,et al.  ATP-sensitive K+ channels mediate alpha 2D-adrenergic receptor contraction of arteriolar smooth muscle and reversal of contraction by hypoxia. , 1995, Circulation research.

[23]  W. Bayliss On the local reactions of the arterial wall to changes of internal pressure , 1902, The Journal of physiology.

[24]  R. Berne,et al.  Longitudinal Gradients in Periarteriolar Oxygen Tension: A Possible Mechanism For the Participation of Oxygen in Local Regulation of Blood Flow , 1970, Circulation research.

[25]  S S Segal,et al.  Microvascular recruitment in hamster striated muscle: role for conducted vasodilation. , 1991, The American journal of physiology.

[26]  Jean-Louis Bény,et al.  Information Networks in the Arterial Wall. , 1999, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[27]  H Kurz,et al.  Structural and biophysical simulation of angiogenesis and vascular remodeling , 2001, Developmental dynamics : an official publication of the American Association of Anatomists.

[28]  J. Marshall The influence of the sympathetic nervous system on individual vessels of the microcirculation of skeletal muscle of the rat , 1982, The Journal of physiology.

[29]  D. C. Miller,et al.  The reversibility of canine vein-graft arterialization. , 1990, Circulation.

[30]  T. Togawa,et al.  Adaptive regulation of wall shear stress optimizing vascular tree function. , 1984, Bulletin of mathematical biology.

[31]  E F Leonard,et al.  Model of structural and functional adaptation of small conductance vessels to arterial hypotension. , 2000, American journal of physiology. Heart and circulatory physiology.

[32]  R. Rivers,et al.  Remote effects of pressure changes in arterioles. , 1995, The American journal of physiology.

[33]  R. Rivers Components of methacholine-initiated conducted vasodilation are unaffected by arteriolar pressure. , 1997, The American journal of physiology.

[34]  N. Holstein-Rathlou,et al.  Conducted vasomotor responses in arterioles: characteristics, mechanisms and physiological significance. , 1999, Acta physiologica Scandinavica.

[35]  A. Pries,et al.  Flow‐dependent regulation of arteriolar diameter in rat skeletal muscle in situ: role of endothelium‐derived relaxing factor and prostanoids. , 1995, The Journal of physiology.

[36]  I. Gibbins,et al.  Noradrenergic and peptidergic innervation of the extrinsic vessels and microcirculation of the rat cremaster muscle. , 1989, Microvascular research.

[37]  A. Pries,et al.  Design principles of vascular beds. , 1995, Circulation research.

[38]  T. Secomb,et al.  Simulation of O2 transport in skeletal muscle: diffusive exchange between arterioles and capillaries. , 1994, The American journal of physiology.

[39]  C D Murray,et al.  The Physiological Principle of Minimum Work: I. The Vascular System and the Cost of Blood Volume. , 1926, Proceedings of the National Academy of Sciences of the United States of America.

[40]  R. Hester,et al.  Differential Inhibition of Functional Dilation of Small Arterioles by Indomethacin and Glibenclamide , 2001, Hypertension.

[41]  H. Dietrich,et al.  Effect of locally applied epinephrine and norepinephrine on blood flow and diameter in capillaries of rat mesentery. , 1989, Microvascular research.

[42]  J. Bassingthwaighte,et al.  Fractal Nature of Regional Myocardial Blood Flow Heterogeneity , 1989, Circulation research.

[43]  I. T. Demchenko,et al.  Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. , 1997, Science.

[44]  J. Martens,et al.  Oxygen sensitivity of cloned voltage-gated K(+) channels expressed in the pulmonary vasculature. , 1999, Circulation research.

[45]  B. Duling,et al.  Interrelations between contracting striated muscle and precapillary microvessels. , 1978, The American journal of physiology.

[46]  David A Tulis,et al.  Flow-induced arterial remodeling in rat mesenteric vasculature. , 1998, American journal of physiology. Heart and circulatory physiology.

[47]  S S Segal,et al.  Propagation of vasomotor responses coordinates arteriolar resistances. , 1989, The American journal of physiology.

[48]  K. Willecke,et al.  Impaired conduction of vasodilation along arterioles in connexin40-deficient mice. , 2000, Circulation research.

[49]  L. Kuo,et al.  Interaction of pressure- and flow-induced responses in porcine coronary resistance vessels. , 1991, The American journal of physiology.

[50]  G. Christ,et al.  Gap junctions in vascular tissues. Evaluating the role of intercellular communication in the modulation of vasomotor tone. , 1996, Circulation research.

[51]  N. Holstein-Rathlou,et al.  Internephron coupling by conducted vasomotor responses in normotensive and spontaneously hypertensive rats. , 1997, The American journal of physiology.

[52]  K. Groebe,et al.  Mathematical modelling of local regulation of blood flow by veno-arterial diffusion of vasoactive metabolites. , 1997, Advances in experimental medicine and biology.

[53]  S. Archer,et al.  Molecular identification of O2 sensors and O2-sensitive potassium channels in the pulmonary circulation. , 2000, Advances in experimental medicine and biology.

[54]  I. Sarelius,et al.  Remote arteriolar dilations in response to muscle contraction under capillaries. , 2000, American journal of physiology. Heart and circulatory physiology.

[55]  I H Sarelius,et al.  Direct coupling between blood flow and metabolism at the capillary level in striated muscle. , 1997, The American journal of physiology.

[56]  T C Skalak,et al.  A Circumferential Stress‐Growth Rule Predicts Arcade Arteriole Formation in a Network Model , 1995, Microcirculation.

[57]  R. D. Hogan,et al.  Vasomotor control: functional hyperemia and beyond. , 1987, Federation proceedings.

[58]  B. Folkow Intravascular pressure as a factor regulating the tone of the small vessels. , 1949, Acta physiologica Scandinavica.

[59]  C G Ellis,et al.  Role of erythrocyte in regulating local O2 delivery mediated by hemoglobin oxygenation. , 2001, American journal of physiology. Heart and circulatory physiology.

[60]  B. Folkow Structure and function of the arteries in hypertension. , 1987, American heart journal.

[61]  D. Welsh,et al.  Spread of vasodilatation and vasoconstriction along feed arteries and arterioles of hamster skeletal muscle , 1999, The Journal of physiology.

[62]  B. Duling,et al.  Microvascular Responses to Alterations in Oxygen Tension , 1972, Circulation research.

[63]  J Dankelman,et al.  Myogenic reactivity and resistance distribution in the coronary arterial tree: a model study. , 2000, American journal of physiology. Heart and circulatory physiology.

[64]  R G Dacey,et al.  Red blood cell regulation of microvascular tone through adenosine triphosphate. , 2000, American journal of physiology. Heart and circulatory physiology.

[65]  J. Liao,et al.  Interaction between adenosine and flow-induced dilation in coronary microvascular network. , 1997, The American journal of physiology.

[66]  Tonya L. Jacobs,et al.  Role for endothelial cell conduction in ascending vasodilatation and exercise hyperaemia in hamster skeletal muscle , 2001, The Journal of physiology.

[67]  S. Rodbard Vascular caliber. , 1975, Cardiology.

[68]  L. Kuo,et al.  Activation of Barium-Sensitive Inward Rectifier Potassium Channels Mediates Remote Dilation of Coronary Arterioles , 2001, Circulation.

[69]  M. Ellsworth,et al.  Conducted vascular responses: communication across the capillary bed. , 1998, Microvascular research.

[70]  R. Hester,et al.  Role of venular endothelium in control of arteriolar diameter during functional hyperemia. , 1994, The American journal of physiology.

[71]  S. Hilton A peripheral arterial conducting mechanism underlying dilatation of the femoral artery and concerned in functional vasodilatation in skeletal muscle , 1959, The Journal of physiology.

[72]  W. Jackson Hypoxia Does Not Activate ATP‐Sensitive K+ Channels in Arteriolar Muscle Cells , 2000, Microcirculation.

[73]  T. Gloe,et al.  Large arterioles in the control of blood flow: role of endothelium-dependent dilation. , 2000, Acta physiologica Scandinavica.

[74]  A. Pries,et al.  Structural adaptation and stability of microvascular networks: theory and simulations. , 1998, American journal of physiology. Heart and circulatory physiology.

[75]  A. Pries,et al.  Resistance to blood flow in microvessels in vivo. , 1994, Circulation research.

[76]  A. Pries,et al.  Venulo-arteriolar communication and propagated response , 1989, Pflügers Archiv.

[77]  H. Dietrich,et al.  Microvascular flow response to localized application of norepinephrine on capillaries in rat and frog skeletal muscle. , 1992, Microvascular research.

[78]  A. Koller,et al.  Endothelium regulates skeletal muscle microcirculation by a blood flow velocity-sensing mechanism. , 1990, The American journal of physiology.

[79]  K. Groebe Precapillary servo control of blood pressure and postcapillary adjustment of flow to tissue metabolic status. A new paradigm for local perfusion regulation. , 1996, Circulation.

[80]  M. Labarbera Principles of design of fluid transport systems in zoology. , 1990, Science.

[81]  S S Segal,et al.  Flow control among microvessels coordinated by intercellular conduction. , 1986, Science.