Robust efficiency and actuator saturation explain healthy heart rate control and variability

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 33, 2014, Pages

  Li, Na ^a   Cruz, Jerry ^b   Chien, Chenghao Simon ^c,d   Sojoudi, Somayeh ^e   Recht, Benjamin ^f   Stone, David ^g   Csete, Marie ^h   Bahmiller, Daniel ^b   Doyle, John C ^b,c,i  

^a HARVARD UNIVERSITY   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c California Institute of Technology   (United States)

^d PHILIPS HEALTHCARE   (United States)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF VIRGINIA   (United States)

^h HUNTINGTON MEDICAL RESEARCH INSTITUTES   (United States)

ⁱ California Institute of Technology   (United States)

Author keywords

Optimal control; Respiratory sinus arrhythmia; System identification

Indexed keywords

ACTUATOR SATURATION; ADULT; ANALYTICAL PARAMETERS; ARTERIAL PRESSURE; ARTICLE; ATHLETE; AUTONOMIC NERVOUS SYSTEM; CARDIOVASCULAR AUTOREGULATION; CIRCULATION; CONTROL SYSTEM; EXERCISE TEST; FEMALE; HEALTH; HEART FUNCTION; HEART RATE CONTROL; HEART RATE VARIABILITY; HUMAN; HUMAN EXPERIMENT; LUNG MINUTE VOLUME; MALE; MATHEMATICAL PHENOMENA; NONLINEAR SYSTEM; NORMAL HUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RESPIRATION CONTROL; ROBUST EFFICIENCY; STRESS; TIME SERIES ANALYSIS; VASCULAR RESISTANCE;

OPTIMAL CONTROL; RESPIRATORY SINUS ARRHYTHMIA; SYSTEM IDENTIFICATION;

ADULT; FEMALE; HEART RATE; HOMEOSTASIS; HUMANS; MALE; MODELS, BIOLOGICAL;

EID: 84906316661     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1401883111     Document Type: Article

References (49)

1. Chandra FA, Buzi G, Doyle JC (2011) Glycolytic oscillations and limits on robust efficiency. Science 333(6039):187-192.
2. Pool R (1989) Is it healthy to be chaotic? Science 243(4891):604-607.
3. Buzsáki G (2006) Rhythms of the Brain (Oxford Univ Press, New York).
4. Glass L (2001) Synchronization and rhythmic processes in physiology. Nature 410(6825):277-284.
5. Buchman TG (2002) The community of the self. Nature 420(6912):246-251.
6. Goldberger AL, et al. (2002) Fractal dynamics in physiology: alterations with disease and aging. Proc Natl Acad Sci USA 99(Suppl 1):2466-2472. (Pubitemid 34165052)
7. Camm AJ, et al.; Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability: Standards of measurement, physiological interpretation and clinical use. Circulation 93(5):1043-1065.
8. Ivanov PC, et al. (1999) Multifractality in human heartbeat dynamics. Nature 399(6735):461-465. (Pubitemid 29258850)
9. Poon CS, Merrill CK (1997) Decrease of cardiac chaos in congestive heart failure. Nature 389(6650):492-495.
10. Moorman JR, et al. (2011) Cardiovascular oscillations at the bedside: Early diagnosis of neonatal sepsis using heart rate characteristics monitoring. Physiol Meas 32(11):1821-1832.
11. Tulppo MP, Mäkikallio TH, Takala TE, Seppänen T, Huikuri HV (1996) Quantitative beat-to-beat analysis of heart rate dynamics during exercise. Am J Physiol 271(1 Pt 2):H244-H252.
12. Yamamoto Y, Hughson RL, Peterson JC (1991) Autonomic control of heart rate during exercise studied by heart rate variability spectral analysis. J Appl Physiol (1985) 71(3):1136-1142.
13. Moorman JR, et al. (2011) Mortality reduction by heart rate characteristic monitoring in very low birth weight neonates: A randomized trial. J Pediatr 159(6):900-906.e1.
14. Akselrod S, et al. (1981) Power spectrum analysis of heart rate fluctuation: A quantitative probe of beat-to-beat cardiovascular control. Science 213(4504):220-222. (Pubitemid 11060568)
15. Mackey MC, Glass L (1977) Oscillation and chaos in physiological control systems. Science 197(4300):287-289. (Pubitemid 8130447)
16. Novak V, et al. (1993) Influence of respiration on heart rate and blood pressure fluctuations. J Appl Physiol 74(2):617-626. (Pubitemid 23078152)
17. Gierałtowski J, Żebrowski JJ, Baranowski R (2012) Multiscale multifractal analysis of heart rate variability recordings with a large number of occurrences of arrhythmia. Phys Rev E Stat Nonlin Soft Matter Phys 85(2 Pt 1):021915.
18. Barabási AL (2009) Scale-free networks: A decade and beyond. Science 325(5939):412-413.
19. Glass L (2009) Introduction to controversial topics in nonlinear science: Is the normal heart rate chaotic? Chaos 19(2):028501.
20. Kluttig A, Kuss O, Greiser KH (2010) Ignoring lack of association of heart rate variability with cardiovascular disease and risk factors: Response to the manuscript "The relationship of autonomic imbalance, heart rate variability cardiovascular disease risk factors" by Julian F. Thayer, Shelby S. Yamamoto, Jos F. Brosschot. Int J Cardiol 145(2):375-376.
21. Young NS, Ioannidis JPA, Al-Ubaydli O (2008) Why current publication practices may distort science. PLoS Med 5(10):e201.
22. Stumpf MPH, Porter MA (2012) Mathematics. Critical truths about power laws. Science 335(6069):665-666.
23. Alderson DL, Doyle JC (2010) Contrasting views of complexity and their implications for network-centric infrastructures. IEEE Transactions on Systems, Man and Cybernetics, Part A: Systems and Humans 40(4):839-852.
24. Ioannidis JPA (2005) Why most published research findings are false. PLoS Med 2(8):e124.
25. Wigertz O (1970) Dynamics of ventilation and heart rate in response to sinusoidal work load in man. J Appl Physiol 29(2):208-218.
26. Warner HR, Cox A (1962) A mathematical model of heart rate control by sympathetic and vagus efferent information. J Appl Physiol 17(2):349-355.
27. Brooks GA, Fahey TD, Baldwin K (2004) Exercise Physiology: Human Bioenergetics and Its Applications (McGraw-Hill, New York).
28. Rowell LB (1993) Human Cardiovascular Control (Oxford Univ Press, New York).
29. Grodins FS, Buell J, Bart AJ (1967) Mathematical analysis and digital simulation of the respiratory control system. J Appl Physiol 22(2):260-276.
30. Guyton A, Hall J (2006) Textbook of Medical Physiology (Elsevier Saunders, Philadelphia), 11th Ed.
31. Hoppensteadt FC, Peskin CS (2002) Modeling and Simulation in Medicine and the Life Sciences (Springer, New York).
32. Batzel JJ, Schneditz D (2007) Cardiovascular and Respiratory Systems: Modeling, Analysis, and Control (Society for Industrial and Applied Mathematics, Philadelphia).
33. Ljung L (1999) System Identification: Theory for the User (Prentice Hall, Upper Saddle River, NJ).
34. Kirk D (2004) Optimal Control Theory: An Introduction (Dover, New York).
35. Doya K, Ishii S, Pouget A, Rao RPN, eds. (2007) Bayesian Brain: Probabilistic Approaches to Neural Coding. (MIT Press, Cambridge, MA).
36. Cheng TM, Savkin AV, Celler BG, Su SW, Wang L (2008) Nonlinear modeling and control of human heart rate response during exercise with various work load intensities. IEEE Trans Biomed Eng 55(11):2499-2508.
37. Mullen TJ, Appel ML, Mukkamala R, Mathias JM, Cohen RJ (1997) System identification of closed-loop cardiovascular control: Effects of posture and autonomic blockade. Am J Physiol 272(1 Pt 2):H448-H461.
38. Paulson OB, Strandgaard S, Edvinsson L (1990) Cerebral autoregulation. Cerebrovasc Brain Metab Rev 2(2):161-192.
39. Bramble DM, Lieberman DE (2004) Endurance running and the evolution of Homo. Nature 432(7015):345-352. (Pubitemid 39551663)
40. Mehlsen J, Pagh K, Nielsen JS, Sestoft L, Nielsen SL (1987) Heart rate response to breathing: Dependency upon breathing pattern. Clin Physiol 7(2):115-124. (Pubitemid 17041298)
41. Hirsch JA, Bishop B (1981) Respiratory sinus arrhythmia in humans: How breathing pattern modulates heart rate. Am J Physiol 241(4):H620-H629.
42. Eckberg DL (1983) Human sinus arrhythmia as an index of vagal cardiac outflow. J Appl Physiol 54(4):961-966.
43. Schäfer C, Rosenblum MG, Kurths J, Abel HH (1998) Heartbeat synchronized with ventilation. Nature 392(6673):239-240.
44. Grossman P, Karemaker J, Wieling W (1991) Prediction of tonic parasympathetic cardiac control using respiratory sinus arrhythmia: The need for respiratory control. Psychophysiology 28(2):201-216.
45. Berntson GG, Cacioppo JT, Quigley KS (1993) Respiratory sinus arrhythmia: Autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology 30(2):183-196. (Pubitemid 23049784)
46. Eckberg DL (2009) Point:counterpoint: Respiratory sinus arrhythmia is due to a central mechanism vs. respiratory sinus arrhythmia is due to the baroreflex mechanism. J Appl Physiol (1985) 106(5):1740-1742, discussion 1744.
47. Doyle JC, Csete M (2011) Architecture, constraints, and behavior. Proc Natl Acad Sci USA 108(Suppl 3):15624-15630.
48. Winslow RL, Trayanova N, Geman D, Miller MI (2012) Computational medicine: Translating models to clinical care. Sci Trans Med 4(158):158rv111.
49. Han K, Nagel JH, Schneiderman N (1992) A continuous representation of heart rate. Engineering in Medicine and Biology Society, 1992. 14th Annual International Conference of the IEEE 2:785-786.