Comparison of chaotic and sinusoidal vasomotion in the regulation of microvascular flow.

OBJECTIVE In order to elucidate the physiological consequences of irregular vasomotion on microvascular flow we have compared the theoretical hydrodynamic consequences of sinusoidal and chaotic fluctuations in the diameter of a single resistance vessel. METHODS In initial experimental studies vasomotion was induced by histamine in isolated rabbit ear resistance arteries (approximately 150 microns diameter) perfused with physiological buffer under both controlled-flow and controlled-pressure conditions. The phase relationships between the observed oscillations in flow and pressure were used to validate a theoretical electrical circuit in which vasomotion was simulated as sinusoidal or as chaotic fluctuations in distal resistance, with compliance incorporated as a parallel capacitance. RESULTS In both the experimental and theoretical situation, oscillations in flow led those in pressure by approximately 90 degrees in controlled-flow mode, whereas they were approximately 180 degrees out of phase in controlled-pressure mode. In the theoretical model an increase in the amplitude of sinusoidal or chaotic diameter fluctuations enhanced flow, but "paradoxically" increased both time-averaged resistance and conductance. The model showed that with sinusoidal fluctuations the "efficiency" of perfusion (i.e., flow/viscous work expended in perfusing the vessel undergoing vasomotion) exhibited a peak whose magnitude was a function of vasomotion amplitude and the proximal capacitance in the circuit, and was attributable to transient release of charge from this capacitance. This phenomenon was not observed in simulations with chaotic vasomotion. Hydrodynamic effects specific to the presence of chaotic dynamics (e.g., abrupt increases or decreases in flow under the variation of a single parameter) were also evident when the intrinsic complexity of the vasomotion, rather than its amplitude, was varied. CONCLUSIONS The model suggests (i) that vasomotion may serve to increase flow, (ii) that conductance provides a more accurate physiological measure of the functional consequences of active vasomotion than resistance, (iii) that chaotic vasomotion dissipates transients more readily than sinusoidal vasomotion, thereby conferring greater stability to microcirculatory perfusion and (iv) that specific modes of chaotic vasomotion may influence flow independently of their amplitude.

[1]  D. Slaaf,et al.  Analysis of vasomotion waveform changes during pressure reduction and adenosine application. , 1990, The American journal of physiology.

[2]  G. Schmid-Schönbein,et al.  New morphological evidence for a mechanism of lymph formation in skeletal muscle. , 1984, Microvascular research.

[3]  M Intaglietta,et al.  Vasomotion patterns in skeletal muscle arterioles during changes in arterial pressure. , 1988, Microvascular research.

[4]  James B. Bassingthwaighte,et al.  Nonlinear Dynamics of Vasomotion , 1993 .

[5]  D H Edwards,et al.  Complexity of chaotic vasomotion is insensitive to flow and pressure but can be regulated by external control. , 1995, The American journal of physiology.

[6]  J. Zehr,et al.  Spontaneous rhythmic contractile behaviour of aortic ring segments isolated from pressure loaded regions of the vasculature. , 1990, Cardiovascular research.

[7]  M. Intaglietta Vasomotor activity, time-dependent fluid exchange and tissue pressure. , 1981, Microvascular research.

[8]  M. Conrad,et al.  1. What is the use of chaos , 1986 .

[9]  Singer,et al.  Controlling a chaotic system. , 1991, Physical review letters.

[10]  B. Folkow,et al.  DESCRIPTION OF THE MYOGENIC HYPOTHESIS. , 1964, Circulation research.

[11]  W. Ditto,et al.  Controlling chaos in the brain , 1994, Nature.

[12]  D. Slaaf,et al.  Effective diameter as a determinant of local vascular resistance in presence of vasomotion. , 1988, The American journal of physiology.

[13]  Celso Grebogi,et al.  Using small perturbations to control chaos , 1993, Nature.

[14]  D J Marsh,et al.  Renal blood flow regulation and arterial pressure fluctuations: a case study in nonlinear dynamics. , 1994, Physiological reviews.

[15]  G. Cokelet,et al.  Fluctuations in microvascular blood flow parameters caused by hemodynamic mechanisms. , 1994, The American journal of physiology.

[16]  G. Coppini,et al.  Hypoxia- or hyperoxia-induced changes in arteriolar vasomotion in skeletal muscle microcirculation. , 1991, The American journal of physiology.

[17]  M. Intaglietta,et al.  Arteriolar vasomotion: implications for tissue ischemia. , 1991, Blood vessels.

[18]  A Garfinkel,et al.  Controlling cardiac chaos. , 1992, Science.

[19]  Timothy W. Secomb,et al.  Effects of Vasomotion on Microcirculatory Mass Transport , 1989 .

[20]  Bai-lin Hao,et al.  Systematics of the Periodic Windows in the Lorenz Model and its Relation with the Antisymmetric Cubic Map , 1988 .

[21]  Alfred Bollinger,et al.  Flux Motion in Peripheral Ischemia1 , 1989 .

[22]  M. Mulvany Possible role of vascular oscillatory activity in the development of high blood pressure in spontaneously hypertensive rats. , 1988, Journal of cardiovascular pharmacology.

[23]  T. M. Griffith,et al.  Fractal analysis of role of smooth muscle Ca2+ fluxes in genesis of chaotic arterial pressure oscillations. , 1994, The American journal of physiology.

[24]  M Intaglietta,et al.  Periodic hemodynamics in skeletal muscle during local arterial pressure reduction. , 1992, Journal of applied physiology.

[25]  D. Edwards,et al.  EDRF suppresses chaotic pressure oscillations in isolated resistance artery without influencing intrinsic complexity. , 1994, The American journal of physiology.

[26]  Colin Sparrow,et al.  The Lorenz equations , 1982 .

[27]  Kestutis Pyragas Continuous control of chaos by self-controlling feedback , 1992 .