Mechano-sensitivity of cardiac pacemaker function: Pathophysiological relevance, experimental implications, and conceptual integration with other mechanisms of rhythmicity

[1]  J. Le Guennec,et al.  A possible mechanism for large stretch-induced increase in [Ca2+]i in isolated guinea-pig ventricular myocytes. , 1996, Cardiovascular research.

[2]  H. Zhang,et al.  Structure–Function Relationship in the Sinus and Atrioventricular Nodes , 2012, Pediatric Cardiology.

[3]  P Kohl,et al.  Mechanosensitive connective tissue: potential influence on heart rhythm. , 1996, Cardiovascular research.

[4]  D. Noble,et al.  The ionic currents underlying pacemaker activity in rabbit sino-atrial node: experimental results and computer simulations , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[5]  P. Kohl,et al.  Cardiac mechano-electric coupling and arrhythmias , 2011 .

[6]  F A Bainbridge,et al.  The influence of venous filling upon the rate of the heart , 1915, The Journal of physiology.

[7]  C. Bolter,et al.  Do Cardiac Neurons Play a Role in the Intrinsic Control of Heart Rate in the Rat? , 2002, Experimental physiology.

[8]  F Sachs,et al.  Stretch‐activated single ion channel currents in tissue‐cultured embryonic chick skeletal muscle. , 1984, The Journal of physiology.

[9]  Satoshi Nishimura,et al.  Responses of single-ventricular myocytes to dynamic axial stretching. , 2008, Progress in biophysics and molecular biology.

[10]  K. Goto,et al.  Effects of lidocaine and verapamil on early afterdepolarizations in isolated rabbit sinoatrial node , 1991, Journal of Anesthesia.

[11]  D. R. Wagoner,et al.  Mechanosensitive gating of atrial ATP-sensitive potassium channels. , 1993 .

[12]  C. Barrett,et al.  The intrinsic rate response of the isolated right atrium of the rat, Rattus norvegicus. , 1998, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[13]  G. Habib,et al.  Valsalva manoeuvre for supraventricular tachycardia in transplanted heart recipient , 1995, The Lancet.

[14]  H. Brown,et al.  Cardiac pacemaking in the sinoatrial node. , 1993, Physiological reviews.

[15]  K. Arakawa,et al.  Electrophysiological Properties in Chronic Lone Atrial Fibrillation , 1991, Circulation.

[16]  D. Allen,et al.  Store-Operated Ca2+ Influx and Expression of TRPC Genes in Mouse Sinoatrial Node , 2007, Circulation research.

[17]  H. Mond,et al.  Electrical remodeling of the atria following loss of atrioventricular synchrony: a long-term study in humans. , 1999, Circulation.

[18]  U. Hoppe,et al.  Direct evidence for calcium conductance of hyperpolarization-activated cyclic nucleotide-gated channels and human native If at physiological calcium concentrations. , 2008, Cardiovascular research.

[19]  M J Lab,et al.  Calcium and mechanically induced potentials in fibroblasts of rat atrium. , 1996, Cardiovascular research.

[20]  Yael Yaniv,et al.  Beat-to-beat Ca(2+)-dependent regulation of sinoatrial nodal pacemaker cell rate and rhythm. , 2011, Journal of molecular and cellular cardiology.

[21]  I. LeGrice,et al.  Fibroblast Network in Rabbit Sinoatrial Node: Structural and Functional Identification of Homogeneous and Heterogeneous Cell Coupling , 2004, Circulation research.

[22]  D. DiFrancesco,et al.  Current-dependent Block of Rabbit Sino-Atrial Node If Channels by Ivabradine , 2002, The Journal of general physiology.

[23]  Hendrick E D J ter Keurs,et al.  The interaction of Ca2+ with sarcomeric proteins: role in function and dysfunction of the heart. , 2012, American journal of physiology. Heart and circulatory physiology.

[24]  A. Zito,et al.  HCN Channels and Heart Rate , 2012, Molecules.

[25]  Rebecca A. B. Burton,et al.  Axial Stretch of Rat Single Ventricular Cardiomyocytes Causes an Acute and Transient Increase in Ca2+ Spark Rate , 2009, Circulation research.

[26]  E. Lakatta,et al.  Rhythmic Ca2+ Oscillations Drive Sinoatrial Nodal Cell Pacemaker Function to Make the Heart Tick , 2005, Annals of the New York Academy of Sciences.

[27]  D. Allen,et al.  Calcium concentration in the myoplasm of skinned ferret ventricular muscle following changes in muscle length. , 1988, The Journal of physiology.

[28]  Klaus A. Deck,et al.  Dehnungseffekte am spontanschlagenden, isolierten Sinusknoten , 1964, Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere.

[29]  D. Hilgemann,et al.  Dual control of cardiac Na+–Ca2+ exchange by PIP2: analysis of the surface membrane fraction by extracellular cysteine PEGylation , 2007, The Journal of physiology.

[30]  David Benoist,et al.  Inhomogeneity in the response to mechanical stimulation: cardiac muscle function and gene expression. , 2008, Progress in biophysics and molecular biology.

[31]  Paul F. Cranefield,et al.  Electrophysiology of the heart , 1976 .

[32]  C. Brooks,et al.  Effect of stretch on the isolated cat sinoatrial node. , 1966, The American journal of physiology.

[33]  R. A. Li,et al.  Gene- and cell-based bio-artificial pacemaker: what basic and translational lessons have we learned? , 2012, Gene Therapy.

[34]  C. Morris,et al.  Mechanosensitivity of N-type calcium channel currents. , 2002, Biophysical journal.

[35]  D. Donald,et al.  Reflexes from the heart and lungs: physiological curiosities or important regulatory mechanisms. , 1978, Cardiovascular research.

[36]  William Craelius,et al.  Stretch activated ion channels in ventricular myocytes , 1988, Bioscience reports.

[37]  A. V. Bezold Uber die physiologischen Wirkungen des essigsauren Veratrins , 1867 .

[38]  M Lei,et al.  Swelling-induced decrease in spontaneous pacemaker activity of rabbit isolated sino-atrial node cells. , 1998, Acta physiologica Scandinavica.

[39]  Denis Noble,et al.  Integrative models of the heart: achievements and limitations , 2001, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[40]  C. Brooks,et al.  Effects of localized stretch of the sinoatrial node region of the dog heart. , 1966, American Journal of Physiology.

[41]  E. Lakatta,et al.  Dynamic interactions of an intracellular Ca2+ clock and membrane ion channel clock underlie robust initiation and regulation of cardiac pacemaker function. , 2008, Cardiovascular research.

[42]  M. Rosen,et al.  Developmental changes in impulse conduction in the canine heart. , 1981, The American journal of physiology.

[43]  U. Ravens,et al.  Mechanical modulation of pacemaker electrophysiology , 2011 .

[44]  J. Dudel,et al.  Das Aktionspotential und Mechanogramm des Herzmuskels unter dem Einfluß der Dehnung , 1954 .

[45]  D. Terrar,et al.  Fundamental importance of Na+–Ca2+ exchange for the pacemaking mechanism in guinea‐pig sino‐atrial node , 2006, The Journal of physiology.

[46]  P Kohl,et al.  Mechanosensitive fibroblasts in the sino‐atrial node region of rat heart: interaction with cardiomyocytes and possible role , 1994, Experimental physiology.

[47]  Y. Li,et al.  Calcium influx through If channels in rat ventricular myocytes. , 2007, American journal of physiology. Cell physiology.

[48]  C. Baumgarten,et al.  Cell volume-sensitive ion channels and transporters in cardiac myocytes , 2011 .

[49]  David Sedmera,et al.  Effects of mechanical loading on early conduction system differentiation in the chick. , 2010, American journal of physiology. Heart and circulatory physiology.

[50]  C. Morris,et al.  Perturbed voltage-gated channel activity in perturbed bilayers: implications for ectopic arrhythmias arising from damaged membrane. , 2012, Progress in biophysics and molecular biology.

[51]  Steven M. Miller,et al.  α1C (Cav1.2) L-type calcium channel mediates mechanosensitive calcium regulation , 2002 .

[52]  R. Myerburg,et al.  Dissimilar length--tension relations of canine ventricular muscle and false tendon: electrophysiologic alterations accompanying deformation. , 1979, Journal of molecular and cellular cardiology.

[53]  Robert H. Anderson Das reizleitungssystem des säugetierherzens: S. Tawara Gustav Fischer, Jena, 1906; 193 pp.; , 1988 .

[54]  D. Rubenstein,et al.  Mechanisms of automaticity in subsidiary pacemakers from cat right atrium. , 1989, Circulation research.

[55]  J. Toyama,et al.  Roles of Cl- channels and Ca2+ mobilization in stretch-induced increase of SA node pacemaker activity. , 1996, The American journal of physiology.

[56]  David S. Rosenbaum,et al.  Circadian rhythms govern cardiac repolarization and arrhythmogenesis , 2012, Nature.

[57]  H. Sugi,et al.  Length-dependent changes of pacemaker frequency in the isolated rabbit sinoatrial node. , 1984, The Japanese journal of physiology.

[58]  D. Kass,et al.  Electrophysiological effect of varied rate and extent of acute in vivo left ventricular load increase. , 1991, Cardiovascular research.

[59]  Albrecht von Haller,et al.  Elementa Physiologiae Corporis Humani , 1997 .

[60]  C. Bolter,et al.  Interaction of the autonomic nervous system with intrinsic cardiac rate regulation in the guinea-pig, Cavia porcellus. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[61]  D. Bers Cardiac excitation–contraction coupling , 2002, Nature.

[62]  Peter Kohl,et al.  Force-length relations in isolated intact cardiomyocytes subjected to dynamic changes in mechanical load. , 2007, American journal of physiology. Heart and circulatory physiology.

[63]  P. Kohl,et al.  Mechano-Electric Feedback in the Heart: Effects on Heart Rate and Rhythm , 2011 .

[64]  M. Boyett,et al.  Ageing‐dependent remodelling of ion channel and Ca2+ clock genes underlying sino‐atrial node pacemaking , 2011, Experimental physiology.

[65]  M. Biel,et al.  Cellular expression and functional characterization of four hyperpolarization-activated pacemaker channels in cardiac and neuronal tissues. , 2001, European journal of biochemistry.

[66]  C. Bolter Intrinsic cardiac rate regulation in the anaesthetized rabbit. , 1994, Acta physiologica Scandinavica.

[67]  Dario DiFrancesco,et al.  What keeps us ticking: a funny current, a calcium clock, or both? , 2009, Journal of molecular and cellular cardiology.

[68]  M J Lab,et al.  Contraction-excitation feedback in myocardium. Physiological basis and clinical relevance. , 1982, Circulation research.

[69]  D. Terrar,et al.  Possible role of calcium release from the sarcoplasmic reticulum in pacemaking in guinea‐pig sino‐atrial node , 1996, Experimental physiology.

[70]  M. Morad,et al.  ‘Pressure–flow‘‐triggered intracellular Ca2+ transients in rat cardiac myocytes: possible mechanisms and role of mitochondria , 2008, The Journal of physiology.

[71]  Jie Huang,et al.  RGS Proteins in Heart: Brakes on the Vagus , 2012, Front. Physio..

[72]  M. Epstein,et al.  Cardiovascular Solid Mechanics: Cells, Tissues, and Organs , 2002 .

[73]  J. Goudevenos,et al.  Segmental wall motion abnormalities alter vulnerability to ventricular ectopic beats associated with acute increases in aortic pressure in patients with underlying coronary artery disease , 1998, Heart.

[74]  A. Kurosky,et al.  TRPC1 forms the stretch-activated cation channel in vertebrate cells , 2005, Nature Cell Biology.

[75]  J. Balligand,et al.  Endogenous nitric oxide mechanisms mediate the stretch dependence of Ca2+ release in cardiomyocytes , 2001, Nature Cell Biology.

[76]  J R BLINKS,et al.  Positive chronotropic effect of increasing right atrial pressure in the isolated mammalian heart. , 1956, The American journal of physiology.

[77]  L. Hondeghem,et al.  Stretch-induced arrhythmias in the isolated canine ventricle. Evidence for the importance of mechanoelectrical feedback. , 1990, Circulation.

[78]  P. Kohl,et al.  Axial stretch enhances sarcoplasmic reticulum Ca2+ leak and cellular Ca2+ reuptake in guinea pig ventricular myocytes: experiments and models. , 2008, Progress in biophysics and molecular biology.

[79]  D. Noble,et al.  Systems Biology: An Approach , 2010, Clinical pharmacology and therapeutics.

[80]  E. White,et al.  The role of calcium in the response of cardiac muscle to stretch. , 1999, Progress in biophysics and molecular biology.

[81]  Michael J. Ackerman,et al.  Ranolazine Decreases Mechanosensitivity of the Voltage-Gated Sodium Ion Channel NaV1.5: A Novel Mechanism of Drug Action , 2012, Circulation.

[82]  T Alexander Quinn,et al.  Systems biology of the heart: hype or hope? , 2011, Annals of the New York Academy of Sciences.

[83]  D. Allen,et al.  Intracellular calcium and Na+‐Ca2+ exchange current in isolated toad pacemaker cells , 1998, The Journal of physiology.

[84]  M R Franz,et al.  Electrophysiological Effects of Myocardial Stretch and Mechanical Determinants of Stretch‐Activated Arrhythmias , 1992, Circulation.

[85]  S Chiba,et al.  Pharmacologic analysis of stretch-induced sinus acceleration of the isolated dog atrium. , 1977, Japanese heart journal.

[86]  A. Reynolds,et al.  On the mechanisms of coupling in adrenaline-induced bigeminy in sensitized hearts. , 1975, Canadian journal of physiology and pharmacology.

[87]  Dario DiFrancesco,et al.  The funny current has a major pacemaking role in the sinus node. , 2012, Heart rhythm.

[88]  C. L. Pathak Autoregulation of chronotropic response of the heart through pacemaker stretch. , 1973, Cardiology.

[89]  A S French,et al.  Stretch-activated cation channels in human fibroblasts. , 1988, Biophysical journal.

[90]  R. Desanctis,et al.  Clinical Spectrum of the Sick Sinus Syndrome , 1972, Circulation.

[91]  M. Romanelli,et al.  Selective pharmacological inhibition of the pacemaker channel isoforms (HCN1-4) as new possible therapeutical targets. , 2011, Current medicinal chemistry.

[92]  N. Chattipakorn,et al.  Heart rate variability in myocardial infarction and heart failure. , 2007, International journal of cardiology.

[93]  C. Bolter Effect of changes in transmural pressure on contraction frequency of the isolated right atrium of the rabbit. , 1996, Acta physiologica Scandinavica.

[94]  M Lei,et al.  Selected contribution: axial stretch increases spontaneous pacemaker activity in rabbit isolated sinoatrial node cells. , 2000, Journal of applied physiology.

[95]  S. Heximer,et al.  Controlling Parasympathetic Regulation of Heart Rate: A Gatekeeper Role for RGS Proteins in the Sinoatrial Node , 2012, Front. Physio..

[96]  G. Billman The cardiac sarcolemmal ATP-sensitive potassium channel as a novel target for anti-arrhythmic therapy. , 2008, Pharmacology & therapeutics.

[97]  E. Lakatta,et al.  Crosstalk between Mitochondrial and Sarcoplasmic Reticulum Ca2+ Cycling Modulates Cardiac Pacemaker Cell Automaticity , 2012, PloS one.

[98]  Craig T. January,et al.  Early Afterdepolarizations: Mechanism of Induction and Block A Role for L‐Type Ca2+ Current , 1989, Circulation research.

[99]  K. Kenno,et al.  Myocardial stretch alters twitch characteristics and Ca2+ loading of sarcoplasmic reticulum in rat ventricular muscle. , 1992, Cardiovascular research.

[100]  Masanori Hirose,et al.  Cardiac Purkinje cells. , 2010, Heart rhythm.

[101]  K. Calloe,et al.  Hypoosmotic cell swelling as a novel mechanism for modulation of cloned HCN2 channels. , 2005, Biophysical journal.

[102]  H Honjo,et al.  Variation in effects of Cs+, UL-FS-49, and ZD-7288 within sinoatrial node. , 1997, The American journal of physiology.

[103]  Peter Kohl,et al.  Species‐ and Preparation‐Dependence of Stretch Effects on Sino‐Atrial Node Pacemaking , 2005, Annals of the New York Academy of Sciences.

[104]  D. Fedida,et al.  The Role of Late INa and Antiarrhythmic Drugs in EAD Formation and Termination in Purkinje Fibers , 2006, Journal of cardiovascular electrophysiology.

[105]  P. Mohler,et al.  New Insights into Genetic Causes of Sinus Node Disease and Atrial Fibrillation , 2008, Journal of cardiovascular electrophysiology.

[106]  K. A. Deck,et al.  Änderungen des Ruhepotentials und der Kabeleigenschaften von Purkinje-Fäden bei der Dehnung , 1964, Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere.

[107]  G. Ferrier The Effects of Tension on Acetylstrophanthidin‐Induced Transient Depolarizations and Aftercontractions in Canine Myocardial and Purkinje Tissues , 1976, Circulation research.

[108]  D. Noble,et al.  Competing Oscillators in Cardiac Pacemaking: Historical Background , 2010, Circulation research.

[109]  Edward G Lakatta,et al.  The emergence of a general theory of the initiation and strength of the heartbeat. , 2006, Journal of pharmacological sciences.

[110]  M. Pinter,et al.  Response of the quiescent heart tube to mechanical stretch in the intact chick embryo. , 1977, Developmental biology.

[111]  Michael R Rosen,et al.  I(f) and the biological pacemaker. , 2006, Pharmacological research.

[112]  H. Seim,et al.  Chronotropic effects of the reversed carboxyl (RC) analogue of acetylcholine (β-homobetaine methylester) at defined intraluminal pressures on isolated right rabbit atria , 1985, Research in experimental medicine. Zeitschrift fur die gesamte experimentelle Medizin einschliesslich experimenteller Chirurgie.

[113]  G. Salama,et al.  The case for the funny current and the calcium clock. , 2012, Heart rhythm.

[114]  D. Brodie,et al.  The Role of Heart Rate Variability in Prognosis for Different Modes of Death in Chronic Heart Failure , 2006, Pacing and clinical electrophysiology : PACE.

[115]  Robert W. Mills,et al.  Ventricular Filling Slows Epicardial Conduction and Increases Action Potential Duration in an Optical Mapping Study of the Isolated Rabbit Heart , 2003, Journal of cardiovascular electrophysiology.

[116]  D. Allen,et al.  The cellular basis of the length-tension relation in cardiac muscle. , 1985, Journal of molecular and cellular cardiology.

[117]  Y. Kurata,et al.  Effects of nicardipine and bupivacaine on early after depolarization in rabbit sinoatrial node cells: a possible mechanism of bupivacaine-induced arrhythmias. , 1999, General pharmacology.

[118]  D. Fedida,et al.  RSD1235 blocks late INa and suppresses early afterdepolarizations and torsades de pointes induced by class III agents. , 2006, Cardiovascular research.

[119]  Olga Solovyova,et al.  Slow force response and auto-regulation of contractility in heterogeneous myocardium. , 2012, Progress in biophysics and molecular biology.

[120]  H. Nakagawa,et al.  Anatomic substrate for idiopathic left ventricular tachycardia. , 1996, Circulation.

[121]  P. Picton,et al.  Discordance between microneurographic and heart-rate spectral indices of sympathetic activity in pulmonary arterial hypertension , 2009, Heart.

[122]  W. Giles,et al.  Identification and properties of an ATP‐sensitive K+ current in rabbit sino‐atrial node pacemaker cells. , 1996, The Journal of physiology.

[123]  H A Fozzard,et al.  Effect of stretch on conduction velocity and cable properties of cardiac Purkinje fibers. , 1979, The American journal of physiology.

[124]  C. Bolter,et al.  Influence of right atrial pressure on the cardiac pacemaker response to vagal stimulation. , 1999, The American journal of physiology.

[125]  Prashanthan Sanders,et al.  Electrical Remodeling of the Atria in Congestive Heart Failure: Electrophysiological and Electroanatomic Mapping in Humans , 2003, Circulation.

[126]  C. Morris,et al.  Dual stretch responses of mHCN2 pacemaker channels: accelerated activation, accelerated deactivation. , 2007, Biophysical journal.

[127]  Robert H. Anderson,et al.  New insights into pacemaker activity: promoting understanding of sick sinus syndrome. , 2007, Circulation.

[128]  H. Keurs,et al.  The interaction of Ca2+ with sarcomeric proteins: role in function and dysfunction of the heart , 2012 .

[129]  P. Reddy,et al.  Respiratory sinus arrhythmia in the denervated human heart. , 1989, Journal of applied physiology.

[130]  D. DiFrancesco,et al.  The “Funny” Pacemaker Current , 2009 .

[131]  P. Sanders,et al.  Effect of Chronic Right Atrial Stretch on Atrial Electrical Remodeling in Patients With an Atrial Septal Defect , 2003, Circulation.

[132]  Yutaka Kagaya,et al.  Sarcomere mechanics in uniform and non-uniform cardiac muscle: a link between pump function and arrhythmias. , 2008, Progress in biophysics and molecular biology.

[133]  C. Morris Pacemaker, potassium, calcium, sodium: stretch modulation of the voltage-gated channels , 2011 .

[134]  D P Zipes,et al.  Pacing-induced chronic atrial fibrillation impairs sinus node function in dogs. Electrophysiological remodeling. , 1996, Circulation.

[135]  C. Bolter,et al.  Tertiapin‐Q removes a mechanosensitive component of muscarinic control of the sinoatrial pacemaker in the rat , 2010, Clinical and experimental pharmacology & physiology.

[136]  R. Kaufmann,et al.  Automatie-fördernde Dehnungseffekte an Purkinje-Fäden, Papillarmuskeln und Vorhoftrabekeln von Rhesus-Affen , 1967, Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere.

[137]  J. Le Guennec,et al.  A new method of attachment of isolated mammalian ventricular myocytes for tension recording: length dependence of passive and active tension. , 1990, Journal of molecular and cellular cardiology.

[138]  K. Hayashi Cardiovascular solid mechanics. Cells, tissues, and organs , 2003 .

[139]  M. Shoda,et al.  Stretch‐activated anion currents of rabbit cardiac myocytes. , 1992, The Journal of physiology.

[140]  M. Lab,et al.  Contribution to heart rate variability by mechanoelectric feedback. Stretch of the sinoatrial node reduces heart rate variability. , 1996, Circulation.

[141]  A Keith,et al.  The Form and Nature of the Muscular Connections between the Primary Divisions of the Vertebrate Heart. , 1907, Journal of anatomy and physiology.

[142]  A. R. Wright,et al.  Cell swelling has differential effects on the rapid and slow components of delayed rectifier potassium current in guinea pig cardiac myocytes , 1995, The Journal of general physiology.

[143]  P. Hunter,et al.  One‐Dimensional Rabbit Sinoatrial Node Models: , 2003, Journal of cardiovascular electrophysiology.

[144]  Y. Uehara,et al.  Sheep cardiac Purkinje fibers: Configurational changes during the cardiac cycle , 2004, Cell and Tissue Research.

[145]  M. Boyett ‘And the beat goes on’ The cardiac conduction system: the wiring system of the heart , 2009, Experimental physiology.

[146]  Michael Foster,et al.  XXIII. The Croonian lecture.—On the rhythm of the heart of the frog, and on the nature of the action of the vagus nerve , 1882, Philosophical Transactions of the Royal Society of London.

[147]  E. Lakatta,et al.  Rhythmic Ryanodine Receptor Ca2+ Releases During Diastolic Depolarization of Sinoatrial Pacemaker Cells Do Not Require Membrane Depolarization , 2004, Circulation research.

[148]  D. Kreitner,et al.  Electrophysiological study of the two main pacemaker mechanisms in the rabbit sinus node. , 1985, Cardiovascular research.

[149]  田淵 淳,et al.  Das Reizleitungssystem des Säugetierherzens : eine anatomisch-histologische Studie über das Atrioventrikularbündel und die Purkinjeschen Fäden , 1906 .

[150]  Henggui Zhang,et al.  SCN5A and sinoatrial node pacemaker function. , 2007, Cardiovascular research.

[151]  D DiFrancesco,et al.  Reciprocal role of the inward currents ib, Na and if in controlling and stabilizing pacemaker frequency of rabbit sino-atrial node cells , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[152]  S. Nattel,et al.  Pharmacological response of quinidine induced early afterdepolarisations in canine cardiac Purkinje fibres: insights into underlying ionic mechanisms. , 1988, Cardiovascular research.

[153]  Edward G Lakatta,et al.  The funny current in the context of the coupled-clock pacemaker cell system. , 2012, Heart rhythm.

[154]  A. Jarisch,et al.  Die afferenten Bahnen des Veratrineffektes in den Herznerven , 1939, Naunyn-Schmiedebergs Archiv für experimentelle Pathologie und Pharmakologie.

[155]  C. Brooks,et al.  Interaction of myogenic and neurogenic mechanisms that control heart rate. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[156]  Stefano Severi,et al.  An updated computational model of rabbit sinoatrial action potential to investigate the mechanisms of heart rate modulation , 2012, The Journal of physiology.

[157]  D. DiFrancesco The cardiac hyperpolarizing-activated current, if. Origins and developments. , 1985, Progress in biophysics and molecular biology.