Skip to main content
Top
Published in: European Journal of Applied Physiology 2/2015

01-02-2015 | Original Article

Cardiovascular and cardiorespiratory phase synchronization in normovolemic and hypovolemic humans

Authors: Qingguang Zhang, Abhijit R. Patwardhan, Charles F. Knapp, Joyce M. Evans

Published in: European Journal of Applied Physiology | Issue 2/2015

Login to get access

Abstract

We investigated whether and how cardiovascular and cardiorespiratory phase synchronization would respond to changes in hydration status and orthostatic stress. Four men and six women were tested during graded head-up tilt (HUT) in both euhydration and dehydration (DEH) conditions. Continuous R–R intervals (RRI), systolic blood pressure (SBP) and respiration were investigated in low (LF 0.04–0.15 Hz) and high (HF 0.15–0.4 Hz) frequency ranges using a phase synchronization index (λ) ranging from 0 (complete lack of interaction) to 1 (perfect interaction) and a directionality index (d), where a positive value of d reflects oscillator 1 driving oscillator 2, and a negative value reflects the opposite driving direction. Surrogate data analysis was used to exclude relationships that occurred by chance. In the LF range, respiration was not synchronized with RRI or SBP, whereas RRI and SBP were phase synchronized. In the HF range, phases among all variables were synchronized. DEH reduced λ among all variables in the HF and did not affect λ between RRI and SBP in the LF region. DEH reduced d between RRI and SBP in the LF and did not affect d among all variables in the HF region. Increasing λ and decreasing d between SBP and RRI were observed in the LF range during HUT. Decreasing λ between SBP and RRI, respiration and RRI, and decreasing d between respiration and SBP were observed in the HF range during HUT. These results show that orthostatic stress disassociated interactions among RRI, SBP and respiration, and that DEH exacerbated the disconnection.
Literature
go back to reference Akselrod S, Gordon D, Madwed JB, Snidman NC, Shannon DC, Cohen RJ (1985) Hemodynamic regulation: investigation by spectral analysis. Am J Physiol 249(4 Pt 2):H867–H875PubMed Akselrod S, Gordon D, Madwed JB, Snidman NC, Shannon DC, Cohen RJ (1985) Hemodynamic regulation: investigation by spectral analysis. Am J Physiol 249(4 Pt 2):H867–H875PubMed
go back to reference Badra LJ, Cooke WH, Hoag JB, Crossman AA, Kuusela TA, Tahvanainen KU, Eckberg DL (2001) Respiratory modulation of human autonomic rhythms. Am J Physiol Heart Circ Physiol 280(6):H2674–H2688PubMed Badra LJ, Cooke WH, Hoag JB, Crossman AA, Kuusela TA, Tahvanainen KU, Eckberg DL (2001) Respiratory modulation of human autonomic rhythms. Am J Physiol Heart Circ Physiol 280(6):H2674–H2688PubMed
go back to reference Cooley RL, Montano N, Cogliati C, van de Borne P, Richenbacher W, Oren R, Somers VK (1998) Evidence for a central origin of the low-frequency oscillation in RR-interval variability. Circulation 98(6):556–561PubMedCrossRef Cooley RL, Montano N, Cogliati C, van de Borne P, Richenbacher W, Oren R, Somers VK (1998) Evidence for a central origin of the low-frequency oscillation in RR-interval variability. Circulation 98(6):556–561PubMedCrossRef
go back to reference Evans JM, Stenger MB, Moore FB, Hinghofer-Szalkay H, Rossler A, Patwardhan AR, Brown DR, Ziegler MG, Knapp CF (2004) Centrifuge training increases presyncopal orthostatic tolerance in ambulatory men. Aviat Space Environ Med 75(10):850–858PubMed Evans JM, Stenger MB, Moore FB, Hinghofer-Szalkay H, Rossler A, Patwardhan AR, Brown DR, Ziegler MG, Knapp CF (2004) Centrifuge training increases presyncopal orthostatic tolerance in ambulatory men. Aviat Space Environ Med 75(10):850–858PubMed
go back to reference Evans JM, Mohney L, Wang SQ, Moore RK, Elayi SC, Stenger MB, Moore FB, Knapp CF (2013) Cardiovascular regulation during body unweighting by lower body positive pressure. Aviat Space Environ Med 84(11):1140–1146. doi:10.3357/Asem.3576.2013 PubMedCrossRef Evans JM, Mohney L, Wang SQ, Moore RK, Elayi SC, Stenger MB, Moore FB, Knapp CF (2013) Cardiovascular regulation during body unweighting by lower body positive pressure. Aviat Space Environ Med 84(11):1140–1146. doi:10.​3357/​Asem.​3576.​2013 PubMedCrossRef
go back to reference Faes L, Nollo G, Porta A (2013a) Mechanisms of causal interaction between short-term RR interval and systolic arterial pressure oscillations during orthostatic challenge. J Appl Physiol (1985) 114(12):1657–1667. doi:10.1152/japplphysiol.01172.2012 Faes L, Nollo G, Porta A (2013a) Mechanisms of causal interaction between short-term RR interval and systolic arterial pressure oscillations during orthostatic challenge. J Appl Physiol (1985) 114(12):1657–1667. doi:10.​1152/​japplphysiol.​01172.​2012
go back to reference Faes L, Porta A, Rossato G, Adami A, Tonon D, Corica A, Nollo G (2013b) Investigating the mechanisms of cardiovascular and cerebrovascular regulation in orthostatic syncope through an information decomposition strategy. Auton Neurosci Basic Clin 178(1–2):76–82. doi:10.1016/j.autneu.2013.02.013 CrossRef Faes L, Porta A, Rossato G, Adami A, Tonon D, Corica A, Nollo G (2013b) Investigating the mechanisms of cardiovascular and cerebrovascular regulation in orthostatic syncope through an information decomposition strategy. Auton Neurosci Basic Clin 178(1–2):76–82. doi:10.​1016/​j.​autneu.​2013.​02.​013 CrossRef
go back to reference Gabor D (1946) Theory of communication. J Inst Electr Eng (Lond) 93(3):429–457 Gabor D (1946) Theory of communication. J Inst Electr Eng (Lond) 93(3):429–457
go back to reference Gilbey MP, Jordan D, Richter DW, Spyer KM (1984) Synaptic mechanisms involved in the inspiratory modulation of vagal cardio-inhibitory neurones in the cat. J Physiol 356:65–78PubMedCentralPubMedCrossRef Gilbey MP, Jordan D, Richter DW, Spyer KM (1984) Synaptic mechanisms involved in the inspiratory modulation of vagal cardio-inhibitory neurones in the cat. J Physiol 356:65–78PubMedCentralPubMedCrossRef
go back to reference Hamner JW, Morin RJ, Rudolph JL, Taylor JA (2001) Inconsistent link between low-frequency oscillations: R–R interval responses to augmented Mayer waves. J Appl Physiol (1985) 90(4):1559–1564 Hamner JW, Morin RJ, Rudolph JL, Taylor JA (2001) Inconsistent link between low-frequency oscillations: R–R interval responses to augmented Mayer waves. J Appl Physiol (1985) 90(4):1559–1564
go back to reference Karavaev AS, Prokhorov MD, Ponomarenko VI, Kiselev AR, Gridnev VI, Ruban EI, Bezruchko BP (2009) Synchronization of low-frequency oscillations in the human cardiovascular system. Chaos 19(3):033112. doi:10.1063/1.3187794 PubMedCrossRef Karavaev AS, Prokhorov MD, Ponomarenko VI, Kiselev AR, Gridnev VI, Ruban EI, Bezruchko BP (2009) Synchronization of low-frequency oscillations in the human cardiovascular system. Chaos 19(3):033112. doi:10.​1063/​1.​3187794 PubMedCrossRef
go back to reference Lackner HK, Papousek I, Batzel JJ, Roessler A, Scharfetter H, Hinghofer-Szalkay H (2011) Phase synchronization of hemodynamic variables and respiration during mental challenge. Int J Psychophysiol Off J Int Organ Psychophysiol 79(3):401–409. doi:10.1016/j.ijpsycho.2011.01.001 CrossRef Lackner HK, Papousek I, Batzel JJ, Roessler A, Scharfetter H, Hinghofer-Szalkay H (2011) Phase synchronization of hemodynamic variables and respiration during mental challenge. Int J Psychophysiol Off J Int Organ Psychophysiol 79(3):401–409. doi:10.​1016/​j.​ijpsycho.​2011.​01.​001 CrossRef
go back to reference Lipsitz LA, Hayano J, Sakata S, Okada A, Morin RJ (1998) Complex demodulation of cardiorespiratory dynamics preceding vasovagal syncope. Circulation 98(10):977–983PubMedCrossRef Lipsitz LA, Hayano J, Sakata S, Okada A, Morin RJ (1998) Complex demodulation of cardiorespiratory dynamics preceding vasovagal syncope. Circulation 98(10):977–983PubMedCrossRef
go back to reference Malliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84(2):482–492PubMedCrossRef Malliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84(2):482–492PubMedCrossRef
go back to reference Malpas SC (2002) Neural influences on cardiovascular variability: possibilities and pitfalls. Am J Physiol Heart Circ Physiol 282(1):H6–H20PubMed Malpas SC (2002) Neural influences on cardiovascular variability: possibilities and pitfalls. Am J Physiol Heart Circ Physiol 282(1):H6–H20PubMed
go back to reference Mrowka R, Cimponeriu L, Patzak A, Rosenblum MG (2003) Directionality of coupling of physiological subsystems: age-related changes of cardiorespiratory interaction during different sleep stages in babies. Am J Physiol Regul Integr Comp Physiol 285(6):R1395–R1401. doi:10.1152/ajpregu.00373.2003 PubMed Mrowka R, Cimponeriu L, Patzak A, Rosenblum MG (2003) Directionality of coupling of physiological subsystems: age-related changes of cardiorespiratory interaction during different sleep stages in babies. Am J Physiol Regul Integr Comp Physiol 285(6):R1395–R1401. doi:10.​1152/​ajpregu.​00373.​2003 PubMed
go back to reference Nollo G, Faes L, Porta A, Antolini R, Ravelli F (2005) Exploring directionality in spontaneous heart period and systolic pressure variability interactions in humans: implications in the evaluation of baroreflex gain. Am J Physiol Heart Circ Physiol 288(4):H1777–H1785. doi:10.1152/ajpheart.00594.2004 PubMedCrossRef Nollo G, Faes L, Porta A, Antolini R, Ravelli F (2005) Exploring directionality in spontaneous heart period and systolic pressure variability interactions in humans: implications in the evaluation of baroreflex gain. Am J Physiol Heart Circ Physiol 288(4):H1777–H1785. doi:10.​1152/​ajpheart.​00594.​2004 PubMedCrossRef
go back to reference Nollo G, Faes L, Antolini R, Porta A (2009) Assessing causality in normal and impaired short-term cardiovascular regulation via nonlinear prediction methods. Philos Trans A Math Phys Eng Sci 367(1892):1423–1440. doi:10.1098/rsta.2008.0275 PubMedCrossRef Nollo G, Faes L, Antolini R, Porta A (2009) Assessing causality in normal and impaired short-term cardiovascular regulation via nonlinear prediction methods. Philos Trans A Math Phys Eng Sci 367(1892):1423–1440. doi:10.​1098/​rsta.​2008.​0275 PubMedCrossRef
go back to reference Pikovsky A, Rosenblum M, Kurths J (2001) Synchronization : a universal concept in nonlinear sciences. The Cambridge nonlinear science series, vol 12. Cambridge University Press, CambridgeCrossRef Pikovsky A, Rosenblum M, Kurths J (2001) Synchronization : a universal concept in nonlinear sciences. The Cambridge nonlinear science series, vol 12. Cambridge University Press, CambridgeCrossRef
go back to reference Porta A, Catai AM, Takahashi AC, Magagnin V, Bassani T, Tobaldini E, van de Borne P, Montano N (2011) Causal relationships between heart period and systolic arterial pressure during graded head-up tilt. Am J Physiol Regul Integr Comp Physiol 300(2):R378–R386. doi:10.1152/ajpregu.00553.2010 PubMedCrossRef Porta A, Catai AM, Takahashi AC, Magagnin V, Bassani T, Tobaldini E, van de Borne P, Montano N (2011) Causal relationships between heart period and systolic arterial pressure during graded head-up tilt. Am J Physiol Regul Integr Comp Physiol 300(2):R378–R386. doi:10.​1152/​ajpregu.​00553.​2010 PubMedCrossRef
go back to reference Riedl M, Suhrbier A, Stepan H, Kurths J, Wessel N (2010) Short-term couplings of the cardiovascular system in pregnant women suffering from pre-eclampsia. Philos Trans A Math Phys Eng Sci 368(1918):2237–2250. doi:10.1098/rsta.2010.0029 PubMedCrossRef Riedl M, Suhrbier A, Stepan H, Kurths J, Wessel N (2010) Short-term couplings of the cardiovascular system in pregnant women suffering from pre-eclampsia. Philos Trans A Math Phys Eng Sci 368(1918):2237–2250. doi:10.​1098/​rsta.​2010.​0029 PubMedCrossRef
go back to reference Rosenblum MG, Pikovsky AS (2001) Detecting direction of coupling in interacting oscillators. Phys Rev E Stat Nonlinear Soft Matter Phys 64(4 Pt 2):045202CrossRef Rosenblum MG, Pikovsky AS (2001) Detecting direction of coupling in interacting oscillators. Phys Rev E Stat Nonlinear Soft Matter Phys 64(4 Pt 2):045202CrossRef
go back to reference Rosenblum MG, Cimponeriu L, Bezerianos A, Patzak A, Mrowka R (2002) Identification of coupling direction: application to cardiorespiratory interaction. Phys Rev E Stat Nonlinear Soft Matter Phys 65(4 Pt 1):041909CrossRef Rosenblum MG, Cimponeriu L, Bezerianos A, Patzak A, Mrowka R (2002) Identification of coupling direction: application to cardiorespiratory interaction. Phys Rev E Stat Nonlinear Soft Matter Phys 65(4 Pt 1):041909CrossRef
go back to reference Rosenblum M, Cimponeriu L, Pikovsky A (2006) Coupled oscillators approach in analysis of bivariate data. In: Schelter B, Winterhalder M, Timmer J (eds) Handbook of time series analysis : recent theoretical developments and applications. Wiley-VCH, Weinheim, pp 159–180CrossRef Rosenblum M, Cimponeriu L, Pikovsky A (2006) Coupled oscillators approach in analysis of bivariate data. In: Schelter B, Winterhalder M, Timmer J (eds) Handbook of time series analysis : recent theoretical developments and applications. Wiley-VCH, Weinheim, pp 159–180CrossRef
go back to reference Rowell LB (1993) Circulatory responses to upright posture. In: Human cardiovascular control. Oxford University Press, New York, pp 39–74 Rowell LB (1993) Circulatory responses to upright posture. In: Human cardiovascular control. Oxford University Press, New York, pp 39–74
go back to reference Taylor JA, Eckberg DL (1996) Fundamental relations between short-term RR interval and arterial pressure oscillations in humans. Circulation 93(8):1527–1532PubMedCrossRef Taylor JA, Eckberg DL (1996) Fundamental relations between short-term RR interval and arterial pressure oscillations in humans. Circulation 93(8):1527–1532PubMedCrossRef
go back to reference Wang X, Krishnamurthy S, Evans J, Bhakta D, Justice L, Bruce E, Patwardhan A (2006) Bispectral analysis as a tool to investigate dynamics of cardiorespiratory physiology. Aviat Space Environ Med 77(2):151–156PubMed Wang X, Krishnamurthy S, Evans J, Bhakta D, Justice L, Bruce E, Patwardhan A (2006) Bispectral analysis as a tool to investigate dynamics of cardiorespiratory physiology. Aviat Space Environ Med 77(2):151–156PubMed
go back to reference Zhang Q, Knapp CF, Stenger MB, Patwardhan AR, Elayi SC, Wang S, Kostas VI, Evans JM (2014) Simulations of gravitational stress on normovolemic and hypovolemic men and women. Aviat Space Environ Med 85(4):407–413. doi:10.3357/ASEM.3828.2014 PubMedCrossRef Zhang Q, Knapp CF, Stenger MB, Patwardhan AR, Elayi SC, Wang S, Kostas VI, Evans JM (2014) Simulations of gravitational stress on normovolemic and hypovolemic men and women. Aviat Space Environ Med 85(4):407–413. doi:10.​3357/​ASEM.​3828.​2014 PubMedCrossRef
Metadata
Title
Cardiovascular and cardiorespiratory phase synchronization in normovolemic and hypovolemic humans
Authors
Qingguang Zhang
Abhijit R. Patwardhan
Charles F. Knapp
Joyce M. Evans
Publication date
01-02-2015
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 2/2015
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-014-3017-4

Other articles of this Issue 2/2015

European Journal of Applied Physiology 2/2015 Go to the issue