Mapping cardiac pacemaker circuits: methodological puzzles of the sinoatrial node optical mapping.

Historically, milestones in science are usually associated with methodological breakthroughs. Likewise, the advent of electrocardiography, microelectrode recordings and more recently optical mapping have ushered in new periods of significance of advancement in elucidating basic mechanisms in cardiac electrophysiology. As with any novel technique, however, data interpretation is challenging and should be approached with caution, as it cannot be simply extrapolated from previously used methodologies and with experience and time eventually becomes validated. A good example of this is the use of optical mapping in the sinoatrial node (SAN): when microelectrode and optical recordings are obtained from the same site in myocardium, significantly different results may be noted with respect to signal morphology and as a result have to be interpreted by a different set of principles. Given the rapid spread of the use of optical mapping, careful evaluation must be made in terms of methodology with respect to interpretation of data gathered by optical sensors from fluorescent potential-sensitive dyes. Different interpretations of experimental data may lead to different mechanistic conclusions. This review attempts to address the origin and interpretation of the "double component" morphology in the optical action potentials obtained from the SAN region. One view is that these 2 components represent distinctive signals from the SAN and atrial cells and can be fully separated with signal processing. A second view is that the first component preceding the phase 0 activation represents the membrane currents and intracellular calcium transients induced diastolic depolarization from the SAN. Although the consensus from both groups is that ionic mechanisms, namely the joint action of the membrane and calcium automaticity, are important in the SAN function, it is unresolved whether the double-component originates from the recording methodology or represents the underlying physiology. This overview aims to advance a common understanding of the basic principles of optical mapping in complex 3D anatomic structures.

[1]  M. Boyett,et al.  Downward gradient in action potential duration along conduction path in and around the sinoatrial node. , 1999, The American journal of physiology.

[2]  Mark R Boyett,et al.  Ageing‐related changes of connexins and conduction within the sinoatrial node , 2004, The Journal of physiology.

[3]  H. Brown,et al.  Pacemaking in rabbit isolated sino‐atrial node cells during Cs+ block of the hyperpolarization‐activated current if. , 1990, The Journal of physiology.

[4]  H. Brown,et al.  How does adrenaline accelerate the heart? , 1979, Nature.

[5]  I. Efimov,et al.  Fluorescent Imaging of a Dual-Pathway Atrioventricular-Nodal Conduction System , 2001, Circulation research.

[6]  R. W. Joyner,et al.  Discontinuous conduction at Purkinje-ventricular muscle junction. , 1996, The American journal of physiology.

[7]  T. C. West,et al.  Ultramicroelectrode recording from the cardiac pacemaker. , 1955, The Journal of pharmacology and experimental therapeutics.

[8]  I Kodama,et al.  Pacemaker Shift in the Rabbit Sinoatrial Node in Response to Vagal Nerve Stimulation , 2001, Experimental physiology.

[9]  Jörg Hüser,et al.  Intracellular Ca2+ release contributes to automaticity in cat atrial pacemaker cells , 2000, The Journal of physiology.

[10]  J. Boineau,et al.  Effect of canine cardiac nerves on heart rate, rhythm, and pacemaker location. , 1986, The American journal of physiology.

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

[12]  V. Tuchin Tissue Optics: Light Scattering Methods and Instruments for Medical Diagnosis , 2000 .

[13]  B. Hoffman,et al.  Electrophysiological evidence for specialized fiber types in rabbit atrium. , 1959, The American journal of physiology.

[14]  Deborah L. Janks,et al.  Averaging over depth during optical mapping of unipolar stimulation , 2002, IEEE Transactions on Biomedical Engineering.

[15]  B. Joung,et al.  Mechanisms of sinoatrial node dysfunction in a canine model of pacing-induced atrial fibrillation. , 2010, Heart rhythm.

[16]  T. N. James,et al.  Anatomy of the sinus node of the dog , 1962, The Anatomical record.

[17]  I. Efimov,et al.  Application of blebbistatin as an excitation-contraction uncoupler for electrophysiologic study of rat and rabbit hearts. , 2007, Heart rhythm.

[18]  M. Taylor,et al.  Reconstruction of the human sinoatrial node , 1967, The Anatomical record.

[19]  Natalia A Trayanova,et al.  The role of photon scattering in optical signal distortion during arrhythmia and defibrillation. , 2007, Biophysical journal.

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

[21]  D. Shah,et al.  Reverse Remodeling of Sinus Node Function After Catheter Ablation of Atrial Fibrillation in Patients With Prolonged Sinus Pauses , 2003, Circulation.

[22]  S. Nattel,et al.  Sinus node dysfunction and hyperpolarization-activated (HCN) channel subunit remodeling in a canine heart failure model. , 2005, Cardiovascular research.

[23]  V. Bennett,et al.  Ankyrin-based cardiac arrhythmias: a new class of channelopathies due to loss of cellular targeting , 2005, Current opinion in cardiology.

[24]  D. Durrer,et al.  Total Excitation of the Isolated Human Heart , 1970, Circulation.

[25]  D. Paterson,et al.  Effects of High Potassium and the Bradycardic Agents ZD7288 and Cesium on Heart Rate of Rabbits and Guinea Pigs , 1995, Journal of cardiovascular pharmacology.

[26]  Richard B Schuessler,et al.  Abnormal Sinus Node Function in Clinical Arrhythmias , 2003, Journal of cardiovascular electrophysiology.

[27]  T. N. James,et al.  Structure and function of the sinus node, AV node and His bundle of the human heart: part I-structure. , 2002, Progress in cardiovascular diseases.

[28]  Halina Dobrzynski,et al.  Differential Expression of Ion Channel Transcripts in Atrial Muscle and Sinoatrial Node in Rabbit , 2006, Circulation research.

[29]  Mya Mya Thu,et al.  Cardiac alternans in embryonic mouse ventricles. , 2008, American journal of physiology. Heart and circulatory physiology.

[30]  A. George,et al.  Congenital sick sinus syndrome caused by recessive mutations in the cardiac sodium channel gene (SCN5A). , 2003, The Journal of clinical investigation.

[31]  D. Noble,et al.  Requirement of neuronal‐ and cardiac‐type sodium channels for murine sinoatrial node pacemaking , 2004, The Journal of physiology.

[32]  E. Lakatta,et al.  Membrane Potential Fluctuations Resulting From Submembrane Ca2+ Releases in Rabbit Sinoatrial Nodal Cells Impart an Exponential Phase to the Late Diastolic Depolarization That Controls Their Chronotropic State , 2006, Circulation research.

[33]  Masao Nishimura,et al.  The role of Ca2+ release from sarcoplasmic reticulum in the regulation of sinoatrial node automaticity , 1996, Heart and Vessels.

[34]  E. Lakatta,et al.  Novel perspectives on the beating rate of the heart. , 2002, Circulation research.

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

[36]  R. P. Thompson,et al.  Optical Mapping of Electrical Activation in the Developing Heart , 2004, Microscopy and Microanalysis.

[37]  T. N. James,et al.  Structure and function of the sinus node, AV node and his bundle of the human heart: part II--function. , 2003, Progress in cardiovascular diseases.

[38]  D. Kass,et al.  Wall Tension Is a Potent Negative Regulator of In Vivo Thrombomodulin Expression , 2003, Circulation Research.

[39]  Tomaso Gnecchi-Ruscone,et al.  Familial sinus bradycardia associated with a mutation in the cardiac pacemaker channel. , 2006, The New England journal of medicine.

[40]  G. Salama,et al.  Optical Imaging of the Heart , 2004, Circulation research.

[41]  M. Boyett,et al.  Declining Into Failure: The Age-Dependent Loss of the L-Type Calcium Channel Within the Sinoatrial Node , 2007, Circulation.

[42]  H Honjo,et al.  Sarcoplasmic Reticulum Ca2+ Release Is Not a Dominating Factor in Sinoatrial Node Pacemaker Activity , 2003, Circulation research.

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

[44]  P. Tchou,et al.  High‐Resolution Fluorescent Imaging Does Not Reveal a Distinct Atrioventricular Nodal Anterior Input Channel (Fast Pathway) in the Rabbit Heart During Sinus Rhythm , 1997, Journal of cardiovascular electrophysiology.

[45]  T. Yuzyuk,et al.  Local cholinergic suppression of pacemaker activity in the rabbit sinoatrial node. , 1998, Journal of cardiovascular pharmacology.

[46]  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.

[47]  A E Becker,et al.  Functional and Morphological Organization of the Rabbit Sinus Node , 1980, Circulation research.

[48]  H. Figulla,et al.  The slow membrane channel as the predominant mediator of the excitation process of the sinoatrial pacemaker cell , 2005, Basic Research in Cardiology.

[49]  Liang Tang,et al.  Intracellular Calcium Dynamics and Acceleration of Sinus Rhythm by &bgr;-Adrenergic Stimulation , 2009, Circulation.

[50]  W. Trautwein,et al.  [Membrane and action potentials of single myocardial fibers of cold and warmblooded animals]. , 1952, Pflugers Archiv fur die gesamte Physiologie des Menschen und der Tiere.

[51]  R B Schuessler,et al.  Multicentric Origin of the Atrial Depolarization Wave: The Pacemaker Complex , 1978, Circulation.

[52]  Edward G Lakatta,et al.  Synergism of coupled subsarcolemmal Ca2+ clocks and sarcolemmal voltage clocks confers robust and flexible pacemaker function in a novel pacemaker cell model. , 2009, American journal of physiology. Heart and circulatory physiology.

[53]  T. Sano,et al.  Spread of Excitation from the Sinus Node , 1965, Circulation research.

[54]  Alan Garny,et al.  An investigation into the role of the optical detection set-up in the recording of cardiac optical mapping signals: A Monte Carlo simulation study , 2009 .

[55]  H. Jongsma,et al.  Electrophysiological features of the mouse sinoatrial node in relation to connexin distribution. , 2001, Cardiovascular research.

[56]  Robert H. Anderson,et al.  Molecular Architecture of the Human Sinus Node: Insights Into the Function of the Cardiac Pacemaker , 2009, Circulation.

[57]  W. J. Meek,et al.  EXPERIMENTS ON THE ORIGIN AND PROPAGATION OF THE IMPULSE IN THE HEART: IV. The Effect of Vagal Stimulation and of Cooling on the Location of the Pacemaker within the Sino-auricular Node , 1914 .

[58]  I. Efimov,et al.  Postganglionic nerve stimulation induces temporal inhibition of excitability in rabbit sinoatrial node. , 2006, American journal of physiology. Heart and circulatory physiology.

[59]  I R Efimov,et al.  Evidence of Three‐Dimensional Scroll Waves with Ribbon‐Shaped Filament as a Mechanism of Ventricular Tachycardia in the Isolated Rabbit Heart , 1999, Journal of cardiovascular electrophysiology.

[60]  A. Wilde,et al.  Contribution of Sodium Channel Mutations to Bradycardia and Sinus Node Dysfunction in LQT3 Families , 2003, Circulation research.

[61]  P B Corr,et al.  Demonstration of a widely distributed atrial pacemaker complex in the human heart. , 1988, Circulation.

[62]  M. Boyett,et al.  Intracellular Ca2+ and pacemaking within the rabbit sinoatrial node: heterogeneity of role and control , 2004, The Journal of physiology.

[63]  R. Coronel,et al.  Ionic Remodeling of Sinoatrial Node Cells by Heart Failure , 2003, Circulation.

[64]  T. N. James,et al.  THE CONNECTING PATHWAYS BETWEEN THE SINUS NODE AND A-V NODE AND BETWEEN THE RIGHT AND THE LEFT ATRIUM IN THE HUMAN HEART. , 1963, American heart journal.

[65]  Masahiro Ogawa,et al.  Left stellate ganglion and vagal nerve activity and cardiac arrhythmias in ambulatory dogs with pacing-induced congestive heart failure. , 2007, Journal of the American College of Cardiology.

[66]  Harold Bien,et al.  Lenses and effective spatial resolution in macroscopic optical mapping. , 2007, Physics in medicine and biology.

[67]  G. Fishman,et al.  Electrical remodeling contributes to complex tachyarrhythmias in connexin43‐deficient mouse hearts , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[68]  N Toda,et al.  The influence of sympathetic stimulation on transmembrane potentials in the S-A node. , 1968, The Journal of pharmacology and experimental therapeutics.

[69]  Ronald Wilders,et al.  Pacemaker activity of the human sinoatrial node: role of the hyperpolarization-activated current, I(f). , 2009, International journal of cardiology.

[70]  P. Sanders,et al.  Remodeling of Sinus Node Function in Patients With Congestive Heart Failure: Reduction in Sinus Node Reserve , 2004, Circulation.

[71]  Matteo E Mangoni,et al.  Genesis and regulation of the heart automaticity. , 2008, Physiological reviews.

[72]  G. Morley,et al.  Understanding conduction of electrical impulses in the mouse heart using high‐resolution video imaging technology , 2001, Microscopy research and technique.

[73]  M. Rosen 15th annual Gordon K. Moe Lecture. Biological pacemaking: in our lifetime? , 2005, Heart Rhythm.

[74]  E. Lakatta,et al.  High Basal Protein Kinase A–Dependent Phosphorylation Drives Rhythmic Internal Ca2+ Store Oscillations and Spontaneous Beating of Cardiac Pacemaker Cells , 2006, Circulation research.

[75]  J. Boineau,et al.  Differential expression of gap junction proteins in the canine sinus node. , 1998, Circulation research.

[76]  F. Cosío,et al.  Atrial Activation Mapping in Sinus Rhythm in the Clinical Electrophysiology Laboratory: , 2004, Journal of cardiovascular electrophysiology.

[77]  S. F. Mironov,et al.  Visualizing excitation waves inside cardiac muscle using transillumination. , 2001, Biophysical journal.

[78]  Michael R. Rosen,et al.  Biological pacemaking: In our lifetime? , 2005 .

[79]  R. Stockwell The Specialized Tissues of the Heart , 1963 .

[80]  R B Schuessler,et al.  Primary negativity does not predict dominant pacemaker location: implications for sinoatrial conduction. , 1995, The American journal of physiology.

[81]  Frederick J Vetter,et al.  Optical Action Potential Upstroke Morphology Reveals Near-Surface Transmural Propagation Direction , 2005, Circulation research.

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

[83]  J. Qu,et al.  Ionic basis of ryanodine's negative chronotropic effect on pacemaker cells isolated from the sinoatrial node. , 1997, American journal of physiology. Heart and circulatory physiology.

[84]  Edward G Lakatta,et al.  &bgr;-Adrenergic Stimulation Modulates Ryanodine Receptor Ca2+ Release During Diastolic Depolarization to Accelerate Pacemaker Activity in Rabbit Sinoatrial Nodal Cells , 2002, Circulation research.

[85]  J. Wikswo,et al.  Examination of optical depth effects on fluorescence imaging of cardiac propagation. , 2003, Biophysical journal.

[86]  I. Seyama Characteristics of the rectifying properties of the sino‐atrial node cell of the rabbit. , 1976, The Journal of physiology.

[87]  E. Lakatta,et al.  Sinoatrial Nodal Cell Ryanodine Receptor and Na + -Ca 2+ Exchanger: Molecular Partners in Pacemaker Regulation , 2001, Circulation research.

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

[89]  T. N. James,et al.  Spontaneous Action Potentials of Cells in the Canine Sinus Node , 1976, Circulation research.

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

[91]  Annalisa Bucchi,et al.  Physiology and pharmacology of the cardiac pacemaker ("funny") current. , 2005, Pharmacology & therapeutics.

[92]  J. Boineau,et al.  Activation Sequence and Potential Distribution Maps Demonstrating Multicentric Atrial Impulse Origin in Dogs , 1984, Circulation research.

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

[94]  A. Wilde,et al.  Expanding Spectrum of Human RYR2-Related Disease: New Electrocardiographic, Structural, and Genetic Features , 2007, Circulation.

[95]  Robert H. Anderson,et al.  New insights into Sick Sinus Syndrome , 2007 .

[96]  T. N. James,et al.  Anatomy of the human sinus node , 1961, The Anatomical record.

[97]  E. Lakatta,et al.  Cyclic Variation of Intracellular Calcium: A Critical Factor for Cardiac Pacemaker Cell Dominance , 2003, Circulation research.

[98]  S. Nattel,et al.  Funny Current Downregulation and Sinus Node Dysfunction Associated With Atrial Tachyarrhythmia: A Molecular Basis for Tachycardia-Bradycardia Syndrome , 2009, Circulation.

[99]  I R Efimov,et al.  High-resolution, three-dimensional fluorescent imaging reveals multilayer conduction pattern in the atrioventricular node. , 1998, Circulation.

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

[101]  Vadim V Fedorov,et al.  Structural and Functional Evidence for Discrete Exit Pathways That Connect the Canine Sinoatrial Node and Atria , 2009, Circulation research.

[102]  Zhengfeng Zhou,et al.  Na(+)‐Ca2+ exchange current in latent pacemaker cells isolated from cat right atrium. , 1993, The Journal of physiology.