Annals of BiomedicalEngineering, Vol.20, pp. 265-268, 1992 Printed in the USA.All rights reserved.
0090-6964/92 $5.00 + .00 1992PergamonPress Ltd.
A Brief History of Bioelectrodes Robert Schmukler Center for Devicesand Radiological Health (CDRH)/FDA (HFZ-133) 12721 Twinbrook Parkway Rockville, MD (Received 8/20/91) The history o f bioelectrodes is intimately associated with electrochemistry in general, through studies on electrode polarization. Electrode polarization was first recognized and studied in the early 1800s, and scientific studies in this area have continued since that time. Experimental and theoretical work on bioelectrodes, electrode polarization, and relevant electrochemistry o f electrode phenomena, is traced f r o m 1826 to Schwan's recent electrode work. Keywords-Bioelectrodes, Electrode polarization, Electrode kinetics.
HISTORY The first thing that may be observed when viewing the history o f bioelectrodes is that the study of bioelectrodes, or for that matter, electrochemistry in general, is enmeshed with studies in electrophysiology. Since the earliest times, the electrical nature of living matter directed developments in electrochemistry, and vice versa. This has been a very fruitful synergy for both areas, with exchange o f information flowing in both directions, to their mutual benefit. To quote Feder: "The history of electrochemistry and bioelectric p h e n o m e n a is linked by electrodes and electrode problems, particularly electrode polarization," (4). Electrode polarization is an interfacial phenomenon occurring at the electrode-electrolyte interface. "To polarize an interface means to alter the potential difference across it, to be polarizable means to be susceptible to changes in potential difference," (1). The first reference to electrode polarization is attributed by Gaston Plante to the 1826 paper by de le Rive, but this paper was somewhat ambiguous and not clear concerning electrode polarization (4). De le Rive studied the behavior of current from the magnetoelectric machine, where the current rapidly alternated direction, e.g., changed direction (8). Another early reference to electrode polarization is from a paper by Henrici Sch6enbein in 1839 (8). In this paper, electrode polarization effects were inThe author would like to thank Prof. Herman Schwan, Prof. Robert de Levie, and Prof. John Stock for providing invaluable references and discussions for this manuscript. The mention of commercialproducts, their sources, or their use in connection with material reported herein is not to be construed as either an implied or actual endorsement of such products by the Department of Health and Human Services. Address correspondenceto Robert Schmukler, CDRH/FDA (HFZ-133) 12721 Twinbrook Parkway, Rockville, MD 20857. 265
266
R. Schmukler
vestigated by measuring with a galvanometer the transient current to a voltage from a Leyden jar into an electrolyte. We know, from Fourier Analysis and Laplace Transforms, that the transient response of a system relates to the AC or sinusoidal behavior of the same system. Polarization should be expected to a greater or lesser extent for both AC and DC perturbations. However, Sch6enbein did not believe in "voltaic polarization," (8). He held that the observed polarization was due to the "usual chemical action," (8). Work on polarization phenomena (both electrode and electrophysiologic) was continued in the 19 th century by Matteucci, 1838 (4,8); Poggendorf, 1841 (8); Daniell and Wheatstone, 1843 (8); Lenz, 1843 (4,8); Horsford, 1847 (5); du Bois Reymond, 1848 (14); Kohlrausch, 1869 (15); Hermann, 1871 (14); and others (4,8,14,15). Discussions and arguments within electrochemistry, concerning electrode polarization, continued from about 1840 to the beginning of the 20 th century, and involved many giants of science at that time. Among them were Ohm (4,8), Faraday (3,8), Poggendorf (8), Ostwald (8,14), Arrhenius (3), Maxwell (3), Helmholtz (14), Nernst (3), and Kohlrausch (15). Electrode processes including electrode polarization and electrode kinetics became focal issues because measurements of charge transport in solution was crucial to understanding ions and electrolytes. Electrode polarization became involved because electrodes were necessary to perform measurements. Faraday's Laws, formulated in 1834 (3), were included in these discussions and arguments, as were studies in electrophysiology. AC technology developed by Kohlrausch in 1869 (15) improved conductance measurements by reducing problems produced by DC electrode polarization effects. In his 1896 book, Ostwald states: " . . . the weakening of the current could be due to generation of a new electromotive force opposed to the original electromotive force, which gives rise to a current. Or alternately, the weakening of the current could be due to the resistance increasing as a consequence of the passage of the current. Both these viewpoints had found zealous defenders" (8). Near the end of the 19 th century, the first distributed element for concentration polarization (distribution of ion densities) was defined in electrochemistry by Warburg in 1899 (6). We know this element today, as the Warburg Impedance in electrode studies. The electrical analog for this impedance is a transmission line impedance (under certain conditions) in series with the electrode interfac e processes that include drops from Nernstian depletion, from Tafel electrode kinetics, and from resistive surface films. The physical kinetic process in the Warburg Impedance is the diffusion of ions down a concentration gradient in electrolytes (2). Both Cremer, in 1900 and Hermann, in 1905, applied the idea of electrode polarization to explain electrophysiologic measurements on nerve cells (2). Studies on electrochemical kinetics in the absence of concentration polarization were done by Tafel in 1905 (3). "Tafel observed that an extra driving voltage, the overpotential ~/, was required to cause electrolysis to proceed at appreciable net rates expressed in terms of current-density, i," (3). The Tafel equation which defines this relationship for overpotential and current density, is one of the most important effects and equations in the group of electrode polarization sources in the absence of concentration polarization. From 1910-12, H6ber studied the conductance of blood. He deduced the existence of a cell membrane, a polarizable element, from his measurements (14). H6ber's deduction followed the hypothesis of a cell membrane, put forward a few years previously, by Bernstein (14). Newberry, 1918 (7), described an AC 4-electrode technique to reduce electrode polarization effects. This technique is used extensively in electrophysiologic measurements. AC measurements on the electrical impedance of blood
A Brief History of Bioelectrodes
267
cells and other biologic samples, commenced shortly after the invention of the Wheatstone bridge (2,9). Further refinements became possible with the introduction o f the vacuum tube ammeter-voltmeter method, work which was done by Philippson in 1921 (2,9). In 1924, Butler (3) and about 1930 Volmer (3), described a formulation for the origin of Tafel's empirical equation. This important relationship is known today as the Butler-Volmer equation (1). Fricke, 1924-25, continued work on conductance measurements of blood and improved the theoretical calculations using Maxwell's suspension equation (2). As a result of his work in 1925, on rabbit muscle, Fricke also became interested in electrode polarization (2). He published a theory of electrolytic polarization later in 1932 (2). In 1926, Wolff investigated the frequency dependence of electrode polarization (2,12) and McClendon, using a Wheatstone bridge, studied the AC impedance of red cells and tissue (2). Gildemeister, 1928, measured the passive electrical properties of cells and found a constant phase angle polarization element (2). K.C. Cole, in 1928, published the first o f his many papers on the electrical impedance of cells, including work on the non-linear properties of nerve membrane (2). Cole's work on nerve membrane eventually led to the famous Hodgkin-Huxley equation (2). His work over the next 40 years, including work on complex dielectrics, led to the Cole-Cole equation, to explain cell membrane impedance (2). The ColeCole equation is a generalization of the constant phase angle element (CPE) (2). The application of Cole's work on complex dielectrics has also been applied to the study of electrode phenomena (6). Mammalian tissue impedance was surveyed in detail in a book edited by Rajewsky in 1938 (2). Included in this book was a systematic survey that Rajewsky and his colleagues had undertaken (14). Also in 1938, Oncley published the first of his papers on electrical measurements o f protein solutions (9). Improvements in the 4-electrode technique for conductance measurements were done by Gordon in 1940 (15). Extensive work on tissue impedance measurements was done by Schwan commencing in 1951 (9). Further studies on biologic membranes were investigated by Schmidtt in 1955 (9). Schwan's continued impedance work elaborated on the ~-dispersion caused by cell membranes (2,9,10). He extended the frequency range of tissue impedance measurements and discovered the a-dispersion effect (10). His extensive survey on the electrical properties of cells and tissues was published in 1957 (2,9,10). Schwan developed and improved the measurement techniques for determining the electrical impedance of biological cells and tissues, which he published in 1963 (9,11). He improved the 4-electrode technique, and adapted it to physiologic measurements (11). Schwan also engaged in extensive studies on polarization phenomena involving platinum electrodes, including platinum black electrodes over both the linear and non-linear range (4,9,11,12). Schwan's investigations into electrode polarization and bioelectric phenomena continue to the present time. REFERENCES
1. Bockris, J.O'M.; Reddy, A.K.N. Modern electrochemistry.Vol. 2: New York: Plenum Press; 1970. 2. Cole, K.S. Membranes ions and impulses. Berkeley:University of California Press; 1972. 3. Conway,B.E. Historicaldevelopmentof the understanding of charge-transferprocessesin electrochemistry. In: Stock, J.T.; Orna, M.V., eds. Electrochemistrypast and present, ACS Syrup.Series390. ACS; 1989. 4. Feder, W. Introduction to bioelectrodes.Annals NYAS: Bioelectrodes. 148; 1968. 5. Horsford, E.N. On the electricalresistanceof liquids. Stock, J.T. trans, from the German article: Uber den electrischenLeitungswiderstandde Flussigkeiten. Annalen der Physik und Chemie 70:238; 1847.
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R. Schmukler
6. Macdonald, J.R. Impedance spectroscopy emphasizing solid materials and systems. New York: John Wiley and Sons; 1987. 7. Newberry, E. A new method for determination of conductivity. J. Chem. Soc. 113:701; 1918. 8. Ostwald, W. Electrochemistry history and theory. Translated from German text: [Electrochemie: Ihre Gesehichte and Lehre. Leipzig: Verlag von Veit & Comp.; 1896], New Delhi: Amerind Publishing Co. Pvt. Ltd.; 1980. 9. Schanne, O.F.; P.-Cerretti, E:R. Impedance measurements in biological cells. New York: J. Wiley and Sons; 1978. 10. Schwan, H.P. Electrical properties of tissue and cell suspensions. In Lawrence, J.H.; Tobias, C.A., eds. Advances in biological and medical physics. Vol. 5. New York: Academic Press; 1957. 11. Schwan, H.P. Determination of biological impedances. In: Nastuk, W.L., ed. Physical techniques in biological research. Vol 6. New York: Academic Press; 1963. 12: Schwan, H.P. Alternating current electrode polarization. Biophysik 3:181; 1966. 13. Schwan, H.P. The development of biomedical engineering: Historical comments and personal observations. IEEE Trans. Biomed. Eng. 31:12; 1984. 14. 'Schwan, H.P.; Takashima, S. Electrical conduction and dielectric behavior in biological systems. Encyclopedia of applied physics. Vol. on Biophysics and Medical Physics. Weinheim, Germany and New York: VCH Publishers; (to be published, 1992). 15. Stock, J.T. Electrochemistry in retrospect an overview. In: Stock, J.T.; Orna, M.V., eds. Electrochemistry past and present. ACS Symp. Series 390. ACS; 1989.
0090-6964/92 $5.00 + .00 1992PergamonPress Ltd.
A Brief History of Bioelectrodes Robert Schmukler Center for Devicesand Radiological Health (CDRH)/FDA (HFZ-133) 12721 Twinbrook Parkway Rockville, MD (Received 8/20/91) The history o f bioelectrodes is intimately associated with electrochemistry in general, through studies on electrode polarization. Electrode polarization was first recognized and studied in the early 1800s, and scientific studies in this area have continued since that time. Experimental and theoretical work on bioelectrodes, electrode polarization, and relevant electrochemistry o f electrode phenomena, is traced f r o m 1826 to Schwan's recent electrode work. Keywords-Bioelectrodes, Electrode polarization, Electrode kinetics.
HISTORY The first thing that may be observed when viewing the history o f bioelectrodes is that the study of bioelectrodes, or for that matter, electrochemistry in general, is enmeshed with studies in electrophysiology. Since the earliest times, the electrical nature of living matter directed developments in electrochemistry, and vice versa. This has been a very fruitful synergy for both areas, with exchange o f information flowing in both directions, to their mutual benefit. To quote Feder: "The history of electrochemistry and bioelectric p h e n o m e n a is linked by electrodes and electrode problems, particularly electrode polarization," (4). Electrode polarization is an interfacial phenomenon occurring at the electrode-electrolyte interface. "To polarize an interface means to alter the potential difference across it, to be polarizable means to be susceptible to changes in potential difference," (1). The first reference to electrode polarization is attributed by Gaston Plante to the 1826 paper by de le Rive, but this paper was somewhat ambiguous and not clear concerning electrode polarization (4). De le Rive studied the behavior of current from the magnetoelectric machine, where the current rapidly alternated direction, e.g., changed direction (8). Another early reference to electrode polarization is from a paper by Henrici Sch6enbein in 1839 (8). In this paper, electrode polarization effects were inThe author would like to thank Prof. Herman Schwan, Prof. Robert de Levie, and Prof. John Stock for providing invaluable references and discussions for this manuscript. The mention of commercialproducts, their sources, or their use in connection with material reported herein is not to be construed as either an implied or actual endorsement of such products by the Department of Health and Human Services. Address correspondenceto Robert Schmukler, CDRH/FDA (HFZ-133) 12721 Twinbrook Parkway, Rockville, MD 20857. 265
266
R. Schmukler
vestigated by measuring with a galvanometer the transient current to a voltage from a Leyden jar into an electrolyte. We know, from Fourier Analysis and Laplace Transforms, that the transient response of a system relates to the AC or sinusoidal behavior of the same system. Polarization should be expected to a greater or lesser extent for both AC and DC perturbations. However, Sch6enbein did not believe in "voltaic polarization," (8). He held that the observed polarization was due to the "usual chemical action," (8). Work on polarization phenomena (both electrode and electrophysiologic) was continued in the 19 th century by Matteucci, 1838 (4,8); Poggendorf, 1841 (8); Daniell and Wheatstone, 1843 (8); Lenz, 1843 (4,8); Horsford, 1847 (5); du Bois Reymond, 1848 (14); Kohlrausch, 1869 (15); Hermann, 1871 (14); and others (4,8,14,15). Discussions and arguments within electrochemistry, concerning electrode polarization, continued from about 1840 to the beginning of the 20 th century, and involved many giants of science at that time. Among them were Ohm (4,8), Faraday (3,8), Poggendorf (8), Ostwald (8,14), Arrhenius (3), Maxwell (3), Helmholtz (14), Nernst (3), and Kohlrausch (15). Electrode processes including electrode polarization and electrode kinetics became focal issues because measurements of charge transport in solution was crucial to understanding ions and electrolytes. Electrode polarization became involved because electrodes were necessary to perform measurements. Faraday's Laws, formulated in 1834 (3), were included in these discussions and arguments, as were studies in electrophysiology. AC technology developed by Kohlrausch in 1869 (15) improved conductance measurements by reducing problems produced by DC electrode polarization effects. In his 1896 book, Ostwald states: " . . . the weakening of the current could be due to generation of a new electromotive force opposed to the original electromotive force, which gives rise to a current. Or alternately, the weakening of the current could be due to the resistance increasing as a consequence of the passage of the current. Both these viewpoints had found zealous defenders" (8). Near the end of the 19 th century, the first distributed element for concentration polarization (distribution of ion densities) was defined in electrochemistry by Warburg in 1899 (6). We know this element today, as the Warburg Impedance in electrode studies. The electrical analog for this impedance is a transmission line impedance (under certain conditions) in series with the electrode interfac e processes that include drops from Nernstian depletion, from Tafel electrode kinetics, and from resistive surface films. The physical kinetic process in the Warburg Impedance is the diffusion of ions down a concentration gradient in electrolytes (2). Both Cremer, in 1900 and Hermann, in 1905, applied the idea of electrode polarization to explain electrophysiologic measurements on nerve cells (2). Studies on electrochemical kinetics in the absence of concentration polarization were done by Tafel in 1905 (3). "Tafel observed that an extra driving voltage, the overpotential ~/, was required to cause electrolysis to proceed at appreciable net rates expressed in terms of current-density, i," (3). The Tafel equation which defines this relationship for overpotential and current density, is one of the most important effects and equations in the group of electrode polarization sources in the absence of concentration polarization. From 1910-12, H6ber studied the conductance of blood. He deduced the existence of a cell membrane, a polarizable element, from his measurements (14). H6ber's deduction followed the hypothesis of a cell membrane, put forward a few years previously, by Bernstein (14). Newberry, 1918 (7), described an AC 4-electrode technique to reduce electrode polarization effects. This technique is used extensively in electrophysiologic measurements. AC measurements on the electrical impedance of blood
A Brief History of Bioelectrodes
267
cells and other biologic samples, commenced shortly after the invention of the Wheatstone bridge (2,9). Further refinements became possible with the introduction o f the vacuum tube ammeter-voltmeter method, work which was done by Philippson in 1921 (2,9). In 1924, Butler (3) and about 1930 Volmer (3), described a formulation for the origin of Tafel's empirical equation. This important relationship is known today as the Butler-Volmer equation (1). Fricke, 1924-25, continued work on conductance measurements of blood and improved the theoretical calculations using Maxwell's suspension equation (2). As a result of his work in 1925, on rabbit muscle, Fricke also became interested in electrode polarization (2). He published a theory of electrolytic polarization later in 1932 (2). In 1926, Wolff investigated the frequency dependence of electrode polarization (2,12) and McClendon, using a Wheatstone bridge, studied the AC impedance of red cells and tissue (2). Gildemeister, 1928, measured the passive electrical properties of cells and found a constant phase angle polarization element (2). K.C. Cole, in 1928, published the first o f his many papers on the electrical impedance of cells, including work on the non-linear properties of nerve membrane (2). Cole's work on nerve membrane eventually led to the famous Hodgkin-Huxley equation (2). His work over the next 40 years, including work on complex dielectrics, led to the Cole-Cole equation, to explain cell membrane impedance (2). The ColeCole equation is a generalization of the constant phase angle element (CPE) (2). The application of Cole's work on complex dielectrics has also been applied to the study of electrode phenomena (6). Mammalian tissue impedance was surveyed in detail in a book edited by Rajewsky in 1938 (2). Included in this book was a systematic survey that Rajewsky and his colleagues had undertaken (14). Also in 1938, Oncley published the first of his papers on electrical measurements o f protein solutions (9). Improvements in the 4-electrode technique for conductance measurements were done by Gordon in 1940 (15). Extensive work on tissue impedance measurements was done by Schwan commencing in 1951 (9). Further studies on biologic membranes were investigated by Schmidtt in 1955 (9). Schwan's continued impedance work elaborated on the ~-dispersion caused by cell membranes (2,9,10). He extended the frequency range of tissue impedance measurements and discovered the a-dispersion effect (10). His extensive survey on the electrical properties of cells and tissues was published in 1957 (2,9,10). Schwan developed and improved the measurement techniques for determining the electrical impedance of biological cells and tissues, which he published in 1963 (9,11). He improved the 4-electrode technique, and adapted it to physiologic measurements (11). Schwan also engaged in extensive studies on polarization phenomena involving platinum electrodes, including platinum black electrodes over both the linear and non-linear range (4,9,11,12). Schwan's investigations into electrode polarization and bioelectric phenomena continue to the present time. REFERENCES
1. Bockris, J.O'M.; Reddy, A.K.N. Modern electrochemistry.Vol. 2: New York: Plenum Press; 1970. 2. Cole, K.S. Membranes ions and impulses. Berkeley:University of California Press; 1972. 3. Conway,B.E. Historicaldevelopmentof the understanding of charge-transferprocessesin electrochemistry. In: Stock, J.T.; Orna, M.V., eds. Electrochemistrypast and present, ACS Syrup.Series390. ACS; 1989. 4. Feder, W. Introduction to bioelectrodes.Annals NYAS: Bioelectrodes. 148; 1968. 5. Horsford, E.N. On the electricalresistanceof liquids. Stock, J.T. trans, from the German article: Uber den electrischenLeitungswiderstandde Flussigkeiten. Annalen der Physik und Chemie 70:238; 1847.
268
R. Schmukler
6. Macdonald, J.R. Impedance spectroscopy emphasizing solid materials and systems. New York: John Wiley and Sons; 1987. 7. Newberry, E. A new method for determination of conductivity. J. Chem. Soc. 113:701; 1918. 8. Ostwald, W. Electrochemistry history and theory. Translated from German text: [Electrochemie: Ihre Gesehichte and Lehre. Leipzig: Verlag von Veit & Comp.; 1896], New Delhi: Amerind Publishing Co. Pvt. Ltd.; 1980. 9. Schanne, O.F.; P.-Cerretti, E:R. Impedance measurements in biological cells. New York: J. Wiley and Sons; 1978. 10. Schwan, H.P. Electrical properties of tissue and cell suspensions. In Lawrence, J.H.; Tobias, C.A., eds. Advances in biological and medical physics. Vol. 5. New York: Academic Press; 1957. 11. Schwan, H.P. Determination of biological impedances. In: Nastuk, W.L., ed. Physical techniques in biological research. Vol 6. New York: Academic Press; 1963. 12: Schwan, H.P. Alternating current electrode polarization. Biophysik 3:181; 1966. 13. Schwan, H.P. The development of biomedical engineering: Historical comments and personal observations. IEEE Trans. Biomed. Eng. 31:12; 1984. 14. 'Schwan, H.P.; Takashima, S. Electrical conduction and dielectric behavior in biological systems. Encyclopedia of applied physics. Vol. on Biophysics and Medical Physics. Weinheim, Germany and New York: VCH Publishers; (to be published, 1992). 15. Stock, J.T. Electrochemistry in retrospect an overview. In: Stock, J.T.; Orna, M.V., eds. Electrochemistry past and present. ACS Symp. Series 390. ACS; 1989.
