Desynchronized vasomotion and desynchronized fiber activation pattern enhance oxygenation in a model of skeletal muscle

Journal of Theoretical Biology

Volumn 259, Issue 2, 2009, Pages 242-252

  Pradhan, Ranjan K ^a   Chakravarthy, V S ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

Author keywords

Capillary network; Chaos; Oxygenation; Synchronization; Vascular regulation; Vasomotion

Indexed keywords

OXYGEN;

MODELING; MUSCLE; OXIDATION; OXYGEN;

ARTICLE; CHEMICAL INTERACTION; MOTONEURON; MUSCLE BLOOD VESSEL; MUSCLE CONTRACTION; NERVE CELL NETWORK; OXYGEN CONSUMPTION; OXYGEN TRANSPORT; OXYGENATION; PRIORITY JOURNAL; PROCESS MODEL; SKELETAL MUSCLE; SYNAPSE; THEORETICAL MODEL; TISSUE OXYGENATION; VASOMOTOR REFLEX;

ANIMALS; CAPILLARIES; FEEDBACK; MICROCIRCULATION; MODELS, BIOLOGICAL; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; NERVE NET; OXYGEN CONSUMPTION; VASOMOTOR SYSTEM;

EID: 67349174281     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2009.02.026     Document Type: Article

References (58)

1. Aalkjaer C., and Nilsson H. Vasomotion: cellular background for the oscillator and for the synchronization of smooth muscle cells. Br. J. Pharmacol. 144 (2005) 605-616
2. Beard D.A., Schenkman K.A., and Feigl E.O. Myocardial oxygenation in isolated hearts predicted by an anatomically realistic microvascular transport model. Am. J. Physiol. Heart Circ. Physiol. 285 (2003) H1826-H1836
3. Beard D.A., and Bassingthwaighte J.B. The fractal nature of myocardial blood flow emerges from a whole-organ model of arterial network. J. Vasc. Res. 37 (2000) 282-296
4. Beard D.A., and Bassingthwaighte J.B. Modeling advection and diffusion of oxygen in complex vascular networks. Ann. Biomed. Eng. 29 (2001) 298-310
5. Bennett R.A., Pittman R.N., and Sullivan S.M. Capillary spatial pattern and muscle fiber geometry in three hamster striated muscles. Am. J. Physiol. 260 (1991) H579-H585
6. Bentley T.B., Meng H., and Pittman R.N. Temperature dependence of oxygen diffusion and consumption in mammalian striated muscle. Am. J. Physiol. 264 (1993) H1825-H1830
7. Bentzer P., Kongstad L., and Grande P.O. Capillary filtration coefficient is independent of number of perfused capillaries in cat skeletal muscle. Am. J. Physiol. Heart Circ. Physiol. 280 (2001) H2697-H2706
8. Berghoff M., Kathpal M., Kilo S., Hilz M.J., and Freeman R. Vascular and neural mechanisms of ACh-mediated vasodilation in the forearm cutaneous microcirculation. J. Appl. Physiol. 92 (2002) 780-788
9. Berridge M.J., and Rapp P.E. A comparative survey of the function, mechanism and control of cellular oscillators. J. Exp. Biol. 81 (1979) 217-279
10. Braverman I.M., Keh A., and Goldminz D. Correlation of laser Doppler wave patterns with underlying microvascular anatomy. J. Invest. Dermatol. 95 (1990) 283-286
11. Buchthal F., and Madsen A. Synchronous activity in normal and atrophic muscle. Electroencephalogr. Clin. Neurophysiol. 2 (1950) 425-444
12. Bullock D., and Grossberg S. Neuromuscular realization of planned trajectories. Neural Networks Suppl. 1 (1989) 329
13. Cardillo C., Kilcoyne C.M., Cannon III R.O., and Panza J.A. Interactions between nitric oxide and endothelin in the regulation of vascular tone of human resistance vessels in vivo. Hypertension 35 (2000) 1237-1241
14. Chaudhuri A., Majeed T., Dinan T., and Behan P.O. Chronic fatigue syndrome: a disorder of central cholinergic transmission. J. Chron. Fatigue Syndr. 3 (1997)
15. Chen G., Suzuki H., and Weston A.H. Acetylcholine releases endothelium-derived hyperpolarizing factor and EDRF from rat blood vessels. Br. J. Pharmacol. 95 (1988) 1165-1174
16. Colantuoni A., Bertuglia S., and Intaglietta M. Quantitation of rhythmic diameter changes in arterial microcirculation. Am. J. Physiol. 246 (1984) H508-H517
17. Dacey Jr. R.G., and Bassett J.E. Cholinergic vasodilation of intracerebral arterioles in rats. Am. J. Physiol. 253 (1987) H1253-H1260
18. Dalakas M.C. Pathogenetic mechanisms of post-polio syndrome: morphological, electrophysiological, virological, and immunological correlations. Ann. N Y Acad. Sci. 753 (1995) 167-185
19. Dash R.K., and Bassingthwaighte J.B. Simultaneous blood-tissue exchange of oxygen, carbon dioxide, bicarbonate, and hydrogen ion. Ann. Biomed. Eng. 34 (2006) 1129-1148
20. De Luca C.J., LeFever R.S., McCue M.P., and Xenakis A.P. Behaviour of human motor units in different muscles during linearly varying contractions. J. Physiol. 329 (1982) 113-128
21. Ellsworth M.L., Popel A.S., and Pittman R.N. Assessment and impact of heterogeneities of convective oxygen transport parameters in capillaries of striated muscle: experimental and theoretical. Microvasc. Res. 35 (1988) 341-362
22. Fagrell B., Fronek A., and Intaglietta M. A microscope-television system for studying flow velocity in human skin capillaries. Am. J. Physiol. 233 (1977) H318-H321
23. Fukuda K., Straus S.E., Hickie I., Sharpe M.C., Dobbins J.G., and Komaroff A. The chronic fatigue syndrome: a comprehensive approach to its definition and study. International Chronic Fatigue Syndrome Study Group. Ann. Intern. Med. 121 (1994) 953-959
24. Gawne A.C., Pham B.T., and Halstead L.S. Electrodiagnostic findings in 108 consecutive patients referred to a post-polio clinic, The value of routine electrodiagnostic studies. Ann. N Y Acad. Sci. 753 (1995) 383-385
25. Goldman D., and Popel A.S. A computational study of the effect of vasomotion on oxygen transport from capillary networks. J. Theor. Biol. 209 (2001) 189-199
26. Griffith T.M. Temporal chaos in the microcirculation. Cardiovasc. Res. 31 (1996) 342-358
27. Griffith T.M., and Edwards D.H. Complexity of chaotic vasomotion is insensitive to flow and pressure but can be regulated by external control. Am. J. Physiol. 269 (1995) H656-H668
28. Groebe K. A versatile model of steady state O2 supply to tissue, application to skeletal muscle. Biophys. J. 57 (1990) 485-498
29. Honig C.R., and Gayeski T.E. Correlation of O2 transport on the micro and macro scale. Int. J. Microcirc. Clin. Exp. 1 (1982) 367-380
30. Hoofd L., and Turek Z. Realistic modelling of capillary spacing in dog gracilis muscle greatly influences the heterogeneity of calculated tissue oxygen pressures. Adv. Exp. Med. Biol. 388 (1996) 333-340
31. Hultborn H., Lindstrom S., and Wigstrom H. On the function of recurrent inhibition in the spinal cord. Exp. Brain Res. 37 (1979) 399-403
32. Izhikevich E.M. Simple model of spiking neurons. IEEE Trans. Neural Network 14 (2003) 1569-1572
33. Johnson P.C. Active and passive determinants of capillary density: a historical perspective. Int. J. Microcirc. Clin. Exp. 15 (1995) 218-222
34. Kamata K., Hosokawa M., Matsumoto T., and Kobayashi T. Acetylcholine-induced vasodilation in the perfused kidney of the streptozotocin-induced diabetic rat: role of prostacyclin. J. Smooth Muscle Res. 42 (2006) 159-170
35. Kellogg Jr. D.L., Zhao J.L., Coey U., and Green J.V. Acetylcholine-induced vasodilation is mediated by nitric oxide and prostaglandins in human skin. J. Appl. Physiol. 98 (2005) 629-632
36. Kogi K., and Hakamada T. Frequency analysis of the surface electromyogram in muscle fatigue. Rodo Kagaku 38 (1962) 519-528
37. Lenman J.A.R., and Ritchie A.E. Clinical Electromyography (1978), Pitman Medial Publishing Co., London
38. Lo A., Fuglevand A.J., and Secomb T.W. Oxygen delivery to skeletal muscle fibers: effects of microvascular unit structure and control mechanisms. Am. J. Physiol. Heart Circ. Physiol. 285 (2003) H955-H963
39. Mahler F., Muheim M.H., Intaglietta M., Bollinger A., and Anliker M. Blood pressure fluctuations in human nailfold capillaries. Am. J. Physiol. 236 (1979) H888-H893
40. Murrant C.L., and Sarelius I.H. Coupling of muscle metabolism and muscle blood flow in capillary units during contraction. Acta Physiol. Scand. 168 (2000) 531-541
41. Nilsson H., and Aalkjaer C. Vasomotion: mechanisms and physiological importance. Mol. Interventions 51 3 (2003) 79-89
42. Norris Jr. F.H. Synchronous fasciculation in motor neuron disease. Arch. Neurol. 13 (1965) 495-500
43. Parthimos D., Edwards D.H., and Griffith T.M. Comparison of chaotic and sinusoidal vasomotion in the regulation of microvascular flow. Cardiovasc. Res. 31 (1996) 388-399
44. Popel A.S., Charny C.K., and Dvinsky A.S. Effect of heterogeneous oxygen delivery on the oxygen distribution in skeletal muscle. Math. Biosci. 81 (1986) 91-113
45. Popel A.S. Theory of oxygen transport to tissue. Crit. Rev. Biomed. Eng. 17 (1989) 257-321
46. Pradhan R.K., Chakravarthy V.S., and Prabhakar A. Effect of chaotic vasomotion in skeletal muscle on tissue oxygenation. Microvasc. Res. 74 (2007) 51-64
47. Pradhan R.K., and Chakravarthy V.S. A computational model that links non-periodic vasomotion to enhanced oxygenation in skeletal muscle. Math. Biosci. 209 (2007) 486-499
48. Prashanth P.S., and Chakravarthy V.S. An oscillator theory of motor unit recruitment. Biol. Cybern. 97 (2007) 351-361
49. Robinson D.M., Ogilvie R.W., Tullson P.C., and Terjung R.L. Increased peak oxygen consumption of trained muscle requires increased electron flux capacity. J. Appl. Physiol. 77 (1994) 1941-1952
50. Sadoyama T., and Miyano H. Frequency analysis of surface EMG to evaluation of muscle fatigue. Eur. J. Appl. Physiol. Occup. Physiol. 47 (1981) 239-246
51. Sato M. Frequency components of the electromyogram led with the bipolar surface electrodes. J. Anthropol. Soc. Nippon 72 (1964) 92-106
52. Schmidt-Lucke C., Borgstrom P., and Schmidt-Lucke J.A. Low frequency flowmotion/(vasomotion) during patho-physiological conditions. Life Sci. 71 (2002) 2713-2728
53. Secomb T.W., Hsu R., Park E.Y., and Dewhirst M.W. Green's function methods for analysis of oxygen delivery to tissue by microvascular networks. Ann. Biomed. Eng. 32 (2004) 1519-1529
54. Secomb T.W., and Pries A.R. Information transfer in microvascular networks. Microcirculation 9 (2002) 377-387
55. Spence V.A., Khan F., and Belch J.J. Enhanced sensitivity of the peripheral cholinergic vascular response in patients with chronic fatigue syndrome. Am. J. Med. 108 (2000) 736-739
56. Trojan D.A., Gendron D., and Cashman N.R. Stimulation frequency-dependent neuromuscular junction transmission defects in patients with prior poliomyelitis. J. Neurol. Sci. 118 (1993) 150-157
57. Tsai A.G., and Intaglietta M. Evidence of flowmotion induced changes in local tissue oxygenation. Int. J. Microcirc. Clin. Exp. 12 (1993) 75-88
58. Yanagisawa M., Kurihara H., Kimura S., Tomobe Y., Kobayashi M., Mitsui Y., Yazaki Y., Goto K., and Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332 (1988) 411-415