Advertisement

Spectral decomposition of cerebrovascular and cardiovascular interactions in patients prone to postural syncope and healthy controls

      Abstract

      We present a framework for the linear parametric analysis of pairwise interactions in bivariate time series in the time and frequency domains, which allows the evaluation of total, causal and instantaneous interactions and connects time- and frequency-domain measures. The framework is applied to physiological time series to investigate the cerebrovascular regulation from the variability of mean cerebral blood flow velocity (CBFV) and mean arterial pressure (MAP), and the cardiovascular regulation from the variability of heart period (HP) and systolic arterial pressure (SAP). We analyze time series acquired at rest and during the early and late phase of head-up tilt in subjects developing orthostatic syncope in response to prolonged postural stress, and in healthy controls. The spectral measures of total, causal and instantaneous coupling between HP and SAP, and between MAP and CBFV, are averaged in the low-frequency band of the spectrum to focus on specific rhythms, and over all frequencies to get time-domain measures. The analysis of cardiovascular interactions indicates that postural stress induces baroreflex involvement, and its prolongation induces baroreflex dysregulation in syncope subjects. The analysis of cerebrovascular interactions indicates that the postural stress enhances the total coupling between MAP and CBFV, and challenges cerebral autoregulation in syncope subjects, while the strong sympathetic activation elicited by prolonged postural stress in healthy controls may determine an increased coupling from CBFV to MAP during late tilt. These results document that the combination of time-domain and spectral measures allows us to obtain an integrated view of cardiovascular and cerebrovascular regulation in healthy and diseased subjects.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Autonomic Neuroscience: Basic and Clinical
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Aaslid R.
        • Lindegaard K.-F.
        • Sorteberg W.
        • Nornes H.
        Cerebral autoregulation dynamics in humans.
        Stroke. 1989; 20: 45-52
        • Akaike H.
        A new look at the statistical model identification.
        IEEE Trans. Autom. Control. 1974; 19: 716-723
        • Anderson T.W.
        • Darling D.A.
        Asymptotic theory of certain" goodness of fit" criteria based on stochastic processes.
        Ann. Math. Stat. 1952; 23: 193-212
        • Baccalá L.A.
        • Sameshima K.
        Frequency domain repercussions of instantaneous Granger causality.
        Entropy. 2021; 23: 1037
        • Bari V.
        • Marchi A.
        • De Maria B.
        • Rossato G.
        • Nollo G.
        • Faes L.
        • Porta A.
        Nonlinear effects of respiration on the crosstalk between cardiovascular and cerebrovascular control systems.
        Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 2016; 374: 20150179
        • Bari V.
        • De Maria B.
        • Mazzucco C.E.
        • Rossato G.
        • Tonon D.
        • Nollo G.
        • Faes L.
        • Porta A.
        Cerebrovascular and cardiovascular variability interactions investigated through conditional joint transfer entropy in subjects prone to postural syncope.
        Physiol. Meas. 2017; 38: 976
        • Bari V.
        • Fantinato A.
        • Vaini E.
        • Gelpi F.
        • Cairo B.
        • De Maria B.
        • Pistuddi V.
        • Ranucci M.
        • Porta A.
        Impact of propofol general anesthesia on cardiovascular and cerebrovascular closed loop variability interactions.
        Biomed. Signal Process. Control. 2021; 68102735
        • Barnett L.
        • Barrett A.B.
        • Seth A.K.
        Granger causality and transfer entropy are equivalent for Gaussian variables.
        Phys. Rev. Lett. 2009; 103238701
        • Baselli G.
        • Cerutti S.
        • Badilini F.
        • Biancardi L.
        • Porta A.
        • Pagani M.
        • Lombardi F.
        • Rimoldi O.
        • Furlan R.
        • Malliani A.
        Model for the assessment of heart period and arterial pressure variability interactions and of respiration influences.
        Med. Biol. Eng. Comput. 1994; 32: 143-152
        • Béchir M.
        • Binggeli C.
        • Corti R.
        • Chenevard R.
        • Spieker L.
        • Ruschitzka F.
        • Lüscher T.F.
        • Noll G.
        Dysfunctional baroreflex regulation of sympathetic nerve activity in patients with vasovagal syncope.
        Circulation. 2003; 107: 1620-1625
        • Brassard P.
        • Labrecque L.
        • Smirl J.D.
        • Tymko M.M.
        • Caldwell H.G.
        • Hoiland R.L.
        • Lucas S.J.E.
        • Denault A.Y.
        • Couture E.J.
        • Ainslie P.N.
        Losing the dogmatic view of cerebral autoregulation.
        Physiol. Rep. 2021; 9e14982
        • Carey B.J.
        • Eames P.J.
        • Panerai R.B.
        • Potter J.F.
        Carbon dioxide, critical closing pressure and cerebral haemodynamics prior to vasovagal syncope in humans.
        Clin. Sci. (Lond). 2001; 101: 351-358
        • Carey B.J.
        • Manktelow B.N.
        • Panerai R.B.
        • Potter J.F.
        Cerebral autoregulatory responses to head-up tilt in normal subjects and patients with recurrent vasovagal syncope.
        Circulation. 2001; 104: 898-902
        • Chen Y.
        • Bressler S.L.
        • Ding M.
        Frequency decomposition of conditional Granger causality and application to multivariate neural field potential data.
        J. Neurosci. Methods. 2006; 150: 228-237
        • Chicharro D.
        On the spectral formulation of Granger causality.
        Biol. Cybern. 2011; 105: 331-347
        • Cipolla M.J.
        Control of Cerebral Blood Flow, in: The Cerebral Circulation.
        2009 (Morgan & Claypool Life Sciences)
        • Claassen J.A.H.R.
        • Meel-van den Abeelen A.S.S.
        • Simpson D.M.
        • Panerai R.B.
        • (CARNet), I.C.A.R.N
        Transfer function analysis of dynamic cerebral autoregulation: a white paper from the international cerebral autoregulation research network.
        J. Cereb. Blood Flow Metab. 2016; 36: 665-680
        • Claydon V.E.
        • Hainsworth R.
        Cerebral autoregulation during orthostatic stress in healthy controls and in patients with posturally related syncope.
        Clin. Auton. Res. 2003; 13: 321-329
        • Cohen M.A.
        • Taylor J.A.
        Short-term cardiovascular oscillations in man: measuring and modelling the physiologies.
        J. Physiol. 2002; 542: 669-683https://doi.org/10.1113/jphysiol.2002.017483
        • Cooke W.H.
        • Hoag J.B.
        • Crossman A.A.
        • Kuusela T.A.
        • Tahvanainen K.U.O.
        • Eckberg D.L.
        Human responses to upright tilt: a window on central autonomic integration.
        J. Physiol. 1999; 517: 617-628
        • Dan D.
        • Hoag J.B.
        • Ellenbogen K.A.
        • Wood M.A.
        • Eckberg D.L.
        • Gilligan D.M.
        Cerebral blood flow velocity declines before arterial pressure in patients with orthostatic vasovagal presyncope.
        J. Am. Coll. Cardiol. 2002; 39: 1039-1045
        • Dickinson C.J.
        • McCubbin J.W.
        Pressor effect of increased cerebrospinal fluid pressure and vertebral artery occlusion with and without anesthesia.
        Circ. Res. 1963; 12: 190-202
        • Diehl R.R.
        • Linden D.
        • Lücke D.
        • Berlit P.
        Spontaneous blood pressure oscillations and cerebral autoregulation.
        Clin. Auton. Res. 1998; 8: 7-12
        • Diehl R.R.
        • Linden D.
        • Chalkiadaki A.
        • Diehl A.
        Cerebrovascular mechanisms in neurocardiogenic syncope with and without postural tachycardia syndrome.
        J. Auton. Nerv. Syst. 1999; 76: 159-166
        • Dinno A.
        Nonparametric pairwise multiple comparisons in independent groups using Dunn’s test.
        Stata J. 2015; 15: 292-300
        • Dwivedi A.K.
        • Mallawaarachchi I.
        • Alvarado L.A.
        Analysis of small sample size studies using nonparametric bootstrap test with pooled resampling method.
        Stat. Med. 2017; 36: 2187-2205
        • Faes L.
        • Widesott L.
        • Del Greco M.
        • Antolini R.
        • Nollo G.
        Causal cross-spectral analysis of heart rate and blood pressure variability for describing the impairment of the cardiovascular control in neurally mediated syncope.
        IEEE Trans. Biomed. Eng. 2005; 53: 65-73
        • Faes L.
        • Erla S.
        • Nollo G.
        Measuring connectivity in linear multivariate processes: definitions, interpretation, and practical analysis.
        Comput. Math. Methods Med. 2012; : 2012
        • Faes L.
        • Erla S.
        • Porta A.
        • Nollo G.
        A framework for assessing frequency domain causality in physiological time series with instantaneous effects.
        Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 2013; 371: 20110618
        • Faes L.
        • Nollo G.
        • Porta A.
        Mechanisms of causal interaction between short-term RR interval and systolic arterial pressure oscillations during orthostatic challenge.
        J. Appl. Physiol. 2013; 114: 1657-1667
        • Faes L.
        • Porta A.
        • Rossato G.
        • Adami A.
        • Tonon D.
        • Corica A.
        • Nollo G.
        Investigating the mechanisms of cardiovascular and cerebrovascular regulation in orthostatic syncope through an information decomposition strategy.
        Auton. Neurosci. Basic Clin. 2013; 178: 76-82https://doi.org/10.1016/j.autneu.2013.02.013
        • Faes L.
        • Stramaglia S.
        • Marinazzo D.
        On the interpretability and computational reliability of frequency-domain Granger causality.
        F1000Research. 2017; : 6
        • Faes L.
        • Gómez-Extremera M.
        • Pernice R.
        • Carpena P.
        • Nollo G.
        • Porta A.
        • Bernaola-Galván P.
        Comparison of methods for the assessment of nonlinearity in short-term heart rate variability under different physiopathological states.
        Chaos Interdiscip. J. Nonlinear Sci. 2019; 29123114https://doi.org/10.1063/1.5115506
        • Faes L.
        • Pernice R.
        • Mijatovic G.
        • Antonacci Y.
        • Krohova J.C.
        • Javorka M.
        • Porta A.
        Information decomposition in the frequency domain: a new framework to study cardiovascular and cardiorespiratory oscillations.
        Philos. Trans. R. Soc. A. 2021; 379: 20200250
        • Furlan R.
        • Porta A.
        • Costa F.
        • Tank J.
        • Baker L.
        • Schiavi R.
        • Robertson D.
        • Malliani A.
        • Mosqueda-Garcia R.
        Oscillatory patterns in sympathetic neural discharge and cardiovascular variables during orthostatic stimulus.
        Circulation. 2000; 101: 886-892
        • Furlan R.
        • Heusser K.
        • Minonzio M.
        • Shiffer D.
        • Cairo B.
        • Tank J.
        • Jordan J.
        • Diedrich A.
        • Gauger P.
        • Zamuner A.R.
        Cardiac and vascular sympathetic baroreflex control during orthostatic pre-syncope.
        J. Clin. Med. 2019; 8: 1434
        • Gelpi F.
        • Bari V.
        • Cairo B.
        • De Maria B.
        • Tonon D.
        • Rossato G.
        • Faes L.
        • Porta A.
        Dynamic cerebrovascular autoregulation in patients prone to postural syncope: comparison of techniques assessing the autoregulation index from spontaneous variability series.
        Auton. Neurosci. 2022; 237102920
        • Geweke J.
        Measurement of linear dependence and feedback between multiple time series.
        J. Am. Stat. Assoc. 1982; 77: 304-313
        • Giller C.A.
        • Mueller M.
        Linearity and non-linearity in cerebral hemodynamics.
        Med. Eng. Phys. 2003; 25: 633-646
        • Granger C.W.J.
        Investigating causal relations by econometric models and cross-spectral methods.
        Econ. J. Econ. Soc. 1969; : 424-438
        • Grubb B.P.
        • Gerard G.
        • Roush K.
        • Temesy-Armos P.
        • Montford P.
        • Elliott L.
        • Hahn H.
        • Brewster P.
        Cerebral vasoconstriction during head-upright tilt-induced vasovagal syncope. A paradoxic and unexpected response.
        Circulation. 1991; 84: 1157-1164
        • Guyenet P.G.
        The sympathetic control of blood pressure.
        Nat. Rev. Neurosci. 2006; 7: 335-346
        • Javorka M.
        • Krohova J.
        • Czippelova B.
        • Turianikova Z.
        • Lazarova Z.
        • Javorka K.
        • Faes L.
        Basic cardiovascular variability signals: mutual directed interactions explored in the information domain.
        Physiol. Meas. 2017; 38: 877-894https://doi.org/10.1088/1361-6579/aa5b77
        • Kapoor W.N.
        Syncope.
        N. Engl. J. Med. 2000; 343: 1856-1862
        • Krohova J.
        • Faes L.
        • Czippelova B.
        • Turianikova Z.
        • Mazgutova N.
        • Pernice R.
        • Busacca A.
        • Marinazzo D.
        • Stramaglia S.
        • Javorka M.
        Multiscale information decomposition dissects control mechanisms of heart rate variability at rest and during physiological stress.
        Entropy. 2019; 21https://doi.org/10.3390/e21050526
        • Krohova J.
        • Faes L.
        • Czippelova B.
        • Pernice R.
        • Turianikova Z.
        • Wiszt R.
        • Mazgutova N.
        • Busacca A.
        • Javorka M.
        Vascular resistance arm of the baroreflex: methodology and comparison with the cardiac chronotropic arm.
        J. Appl. Physiol. 2020; 128: 1310-1320https://doi.org/10.1152/japplphysiol.00512.2019
        • La Rovere M.T.
        • Bigger Jr., J.T.
        • Marcus F.I.
        • Mortara A.
        • Schwartz P.J.
        • Investigators, A. (Autonomic T. and R.A.M.I.)
        Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction.
        Lancet. 1998; 351: 478-484
        • Lanfranchi P.A.
        • Somers V.K.
        Arterial baroreflex function and cardiovascular variability: interactions and implications.
        Am. J. Physiol. Integr. Comp. Physiol. 2002; 283: R815-R826
        • Lassen N.A.
        Cerebral blood flow and oxygen consumption in man.
        Physiol. Rev. 1959; 39: 183-238
        • Laude D.
        • Elghozi J.-L.
        • Girard A.
        • Bellard E.
        • Bouhaddi M.
        • Castiglioni P.
        • Cerutti C.
        • Cividjian A.
        • Di Rienzo M.
        • Fortrat J.-O.
        Comparison of various techniques used to estimate spontaneous baroreflex sensitivity (the EuroBaVar study).
        Am. J. Physiol. Integr. Comp. Physiol. 2004; 286: R226-R231
        • Lee S.H.
        • Yang J.H.
        • Yim H.R.
        • Park J.
        • Park S.
        • Park K.
        • On Y.K.
        • Kim J.S.
        Hemodynamic parameters and baroreflex sensitivity during head-up tilt test in patients with neurally mediated syncope.
        Pacing Clin. Electrophysiol. 2017; 40: 1454-1461
        • Levine B.D.
        • Giller C.A.
        • Lane L.D.
        • Buckey J.C.
        • Blomqvist C.G.
        Cerebral versus systemic hemodynamics during graded orthostatic stress in humans.
        Circulation. 1994; 90: 298-306
        • Magagnin V.
        • Bassani T.
        • Bari V.
        • Turiel M.
        • Maestri R.
        • Pinna G.D.
        • Porta A.
        Non-stationarities significantly distort short-term spectral, symbolic and entropy heart rate variability indices.
        Physiol. Meas. 2011; 32: 1775
        • Malik M.
        • Bigger J.T.
        • Camm A.J.
        • Kleiger R.E.
        • Malliani A.
        • Moss A.J.
        • Schwartz P.J.
        Heart rate variabilityStandards of measurement, physiological interpretation, and clinical use.
        Eur. Heart J. 1996; 17: 354-381
        • Martin K.
        • Bates G.
        • Whitehouse W.P.
        Transient loss of consciousness and syncope in children and young people: what you need to know.
        Arch. Dis. Childhood-Education Pract. 2010; 95: 66-72
        • McBryde F.D.
        • Malpas S.C.
        • Paton J.F.R.
        Intracranial mechanisms for preserving brain blood flow in health and disease.
        Acta Physiol. 2017; 219: 274-287
        • Medow M.S.
        • Del Pozzi A.T.
        • Messer Z.R.
        • Terilli C.
        • Stewart J.M.
        Altered oscillatory cerebral blood flow velocity and autoregulation in postural tachycardia syndrome.
        Front. Physiol. 2014; 5: 234
        • Montano N.
        • Ruscone T.G.
        • Porta A.
        • Lombardi F.
        • Pagani M.
        • Malliani A.
        Power spectrum analysis of heart rate variability to assess the changes in sympathovagal balance during graded orthostatic tilt.
        Circulation. 1994; 90: 1826-1831
        • Mosqueda-Garcia R.
        • Furlan R.
        • Fernandez-Violante R.
        • Desai T.
        • Snell M.
        • Jarai Z.
        • Ananthram V.
        • Robertson R.M.
        • Robertson D.
        Sympathetic and baroreceptor reflex function in neurally mediated syncope evoked by tilt.
        J. Clin. Invest. 1997; 99: 2736-2744
        • Nollo G.
        • Faes L.
        • Pellegrini B.
        • Porta A.
        • Antolini R.
        Synchronization index for quantifying nonlinear causal coupling between RR interval and systolic arterial pressure after myocardial infarction.
        in: Computers in Cardiology. Vol. 27. IEEE, 2000: 143-146 (Cat. 00CH37163)
        • Nollo G.
        • Faes L.
        • Porta A.
        • Pellegrini B.
        • Ravelli F.
        • Del Greco M.
        • Disertori M.
        • Antolini R.
        Evidence of unbalanced regulatory mechanism of heart rate and systolic pressure after acute myocardial infarction.
        Am. J. Physiol. Heart Circ. Physiol. 2002; 283: 1200-1207https://doi.org/10.1152/ajpheart.00882.2001
        • Nollo G.
        • Faes L.
        • Antolini R.
        • Porta A.
        Assessing causality in normal and impaired short-term cardiovascular regulation via nonlinear prediction methods.
        Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 2009; 367: 1423-1440
        • Novak P.
        Cerebral blood flow, heart rate, and blood pressure patterns during the tilt test in common orthostatic syndromes.
        Neurosci. J. 2016; 2016
        • Numan T.
        • Bain A.R.
        • Hoiland R.L.
        • Smirl J.D.
        • Lewis N.C.
        • Ainslie P.N.
        Static autoregulation in humans: a review and reanalysis.
        Med. Eng. Phys. 2014; 36: 1487-1495
        • Nuzzi D.
        • Stramaglia S.
        • Javorka M.
        • Marinazzo D.
        • Porta A.
        • Faes L.
        Extending the spectral decomposition of Granger causality to include instantaneous influences: application to the control mechanisms of heart rate variability.
        Philos. Trans. R. Soc. A. 2021; 379: 20200263
        • Ocon A.J.
        • Kulesa J.
        • Clarke D.
        • Taneja I.
        • Medow M.S.
        • Stewart J.M.
        Increased phase synchronization and decreased cerebral autoregulation during fainting in the young.
        Am. J. Physiol. Circ. Physiol. 2009; 297: H2084-H2095
        • Panerai R.B.
        • White R.P.
        • Markus H.S.
        • Evans D.H.
        Grading of cerebral dynamic autoregulation from spontaneous fluctuations in arterial blood pressure.
        Stroke. 1998; 29: 2341-2346
        • Paulson O.B.
        • Strandgaard S.
        • Edvinsson L.
        Cerebral autoregulation.
        Cerebrovasc. Brain Metab. Rev. 1990; 2: 161-192
        • Pernice R.
        • Sparacino L.
        • Nollo G.
        • Stivala S.
        • Busacca A.
        • Faes L.
        Comparison of frequency domain measures based on spectral decomposition for spontaneous baroreflex sensitivity assessment after acute myocardial infarction.
        Biomed. Signal Process. Control. 2021; 68102680
        • Porta A.
        • Elstad M.
        Probing the cardiac arm of the baroreflex and complementary branches.
        Front. Neurosci. 2020; 13: 1422
        • Porta A.
        • Faes L.
        Assessing Causality in Brain Dynamics and Cardiovascular Control.
        2013
        • Porta A.
        • Furlan R.
        • Rimoldi O.
        • Pagani M.
        • Malliani A.
        • Van De Borne P.
        Quantifying the strength of the linear causal coupling in closed loop interacting cardiovascular variability signals.
        Biol. Cybern. 2002; 86: 241-251
        • Porta A.
        • Tobaldini E.
        • Guzzetti S.
        • Furlan R.
        • Montano N.
        • Gnecchi-Ruscone T.
        Assessment of cardiac autonomic modulation during graded head-up tilt by symbolic analysis of heart rate variability.
        Am. J. Physiol. Circ. Physiol. 2007; 293: H702-H708https://doi.org/10.1152/ajpheart.00006.2007
        • Porta A.
        • Catai A.M.
        • Takahashi A.C.M.
        • Magagnin V.
        • Bassani T.
        • Tobaldini E.
        • Van De Borne P.
        • Montano N.
        Causal relationships between heart period and systolic arterial pressure during graded head-up tilt.
        Am. J. Physiol. Integr. Comp. Physiol. 2011; 300: R378-R386
        • Porta A.
        • Bassani T.
        • Bari V.
        • Pinna G.D.
        • Maestri R.
        • Guzzetti S.
        Accounting for respiration is necessary to reliably infer Granger causality from cardiovascular variability series.
        IEEE Trans. Biomed. Eng. 2012; 59: 832-841https://doi.org/10.1109/TBME.2011.2180379
        • Porta A.
        • Bari V.
        • Bassani T.
        • Marchi A.
        • Pistuddi V.
        • Ranucci M.
        Model-based causal closed-loop approach to the estimate of baroreflex sensitivity during propofol anesthesia in patients undergoing coronary artery bypass graft.
        J. Appl. Physiol. 2013; 115: 1032-1042
        • Porta A.
        • Gelpi F.
        • Bari V.
        • Cairo B.
        • De Maria B.
        • Panzetti C.M.
        • Cornara N.
        • Bertoldo E.G.
        • Fiolo V.
        • Callus E.
        Monitoring the evolution of asynchrony between mean arterial pressure and mean cerebral blood flow via cross-entropy methods.
        Entropy. 2022; 24: 80
        • Rahman F.
        • Pechnik S.
        • Gross D.
        • Sewell L.
        • Goldstein D.S.
        Low frequency power of heart rate variability reflects baroreflex function, not cardiac sympathetic innervation.
        Clin. Auton. Res. 2011; 21: 133-141
        • Saleem S.
        • Teal P.D.
        • Howe C.A.
        • Tymko M.M.
        • Ainslie P.N.
        • Tzeng Y.-C.
        Is the Cushing mechanism a dynamic blood pressure-stabilizing system? Insights from Granger causality analysis of spontaneous blood pressure and cerebral blood flow.
        Am. J. Physiol. Integr. Comp. Physiol. 2018; 315: R484-R495
        • Schiatti L.
        • Nollo G.
        • Rossato G.
        • Faes L.
        Extended Granger causality: a new tool to identify the structure of physiological networks.
        Physiol. Meas. 2015; 36: 827
        • Serrador J.M.
        • Hughson R.L.
        • Kowalchuk J.M.
        • Bondar R.L.
        • Gelb A.W.
        Cerebral blood flow during orthostasis: role of arterial CO2.
        Am. J. Physiol. Integr. Comp. Physiol. 2006; 290: R1087-R1093
        • Shanlin R.J.
        • Sole M.J.
        • Rahimifar M.
        • Tator C.H.
        • Factor S.M.
        Increased intracranial pressure elicils hypertension, increased sympathetic activity, electrocardiographic abnormalities and myocardial damage in rats.
        J. Am. Coll. Cardiol. 1988; 12: 727-736
        • Silvani S.
        • Padoan G.
        • Guidi A.R.
        • Bianchedi G.
        • Maresta A.
        Cerebral vasoconstriction in neurally mediated syncope: relationship with type of head-up tilt test response.
        Ital. Hear. J. 2003; 4: 768-775
        • Tan C.O.
        • Taylor J.A.
        Integrative physiological and computational approaches to understand autonomic control of cerebral autoregulation.
        Exp. Physiol. 2014; 99: 3-15
        • Tiecks F.P.
        • Lam A.M.
        • Aaslid R.
        • Newell D.W.
        Comparison of static and dynamic cerebral autoregulation measurements.
        Stroke. 1995; 26: 1014-1019
        • Töyry J.P.
        • Kuikka J.T.
        • Länsimies E.A.
        Regional cerebral perfusion in cardiovascular reflex syncope.
        Eur. J. Nucl. Med. 1997; 24: 215-218
        • Tzeng Y.-C.
        • MacRae B.A.
        • Ainslie P.N.
        • Chan G.S.H.
        Fundamental relationships between blood pressure and cerebral blood flow in humans.
        J. Appl. Physiol. 2014; 117: 1037-1048
        • Van Lieshout J.J.
        • Wieling W.
        • Karemaker J.M.
        • Secher N.H.
        Syncope, cerebral perfusion, and oxygenation.
        J. Appl. Physiol. 2003; 94: 833-848
        • Voss A.
        • Schulz S.
        • Schroeder R.
        • Baumert M.
        • Caminal P.
        Methods derived from nonlinear dynamics for analysing heart rate variability.
        Philos. Trans. Math. Phys. Eng. Sci. 2009; : 277-296
        • Westerhof N.
        • Lankhaar J.-W.
        • Westerhof B.E.
        The arterial windkessel.
        Med. Biol. Eng. Comput. 2009; 47: 131-141
        • Wobbrock J.O.
        • Findlater L.
        • Gergle D.
        • Higgins J.J.
        The aligned rank transform for nonparametric factorial analyses using only anova procedures.
        in: Proceedings of the SIGCHI Conference on Human Factors in Computing Systems. 2011: 143-146
        • Yap B.W.
        • Sim C.H.
        Comparisons of various types of normality tests.
        J. Stat. Comput. Simul. 2011; 81: 2141-2155
        • Zhang R.
        • Zuckerman J.H.
        • Giller C.A.
        • Levine B.D.
        • Zuckerman J.H.
        • Giller C.A.
        Transfer function analysis of dynamic cerebral autoregulation in humans.
        Am. J. Physiol. Circ. Physiol. 1998; 274: H233-H241
        • Zhang R.
        • Zuckerman J.H.
        • Levine B.D.
        Deterioration of cerebral autoregulation during orthostatic stress: insights from the frequency domain.
        J. Appl. Physiol. 1998; 85: 1113-1122