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Bernstein's Long Path to Membrane Theory: Radical Change and Conservation in Nineteenth-Century German Electrophysiology
Abstract
This article aims at illustrating the historical circumstances that led Julius Bernstein in 190213.
Bernstein , J and
Tschermak , A . 1902. Ueber die Beziehung der negativen Schwankung des Muskelstromes zur Arbeitsleistung des Muskels. Pflügers Arch, 89: 289–331. View all references to formulate a membrane theory on resting current in muscle and nerve fibers. It was a truly paradigm shift in research into bioelectrical phenomena, if qualified by the observation that, besides Bernstein, many other electrophysiologists between 1890 and 1902 borrowed ideas from the recent ionistic approach in the physical-chemistry domain. But Bernstein's subjective perception of that paradigm shift was that it constituted a mere reinterpretation of the so-called preexistence theory advanced by his teacher Emil du Bois-Reymond in the first half of the nineteenth century.
... He suggested that excitation was the result of a change in permeability of the 2 Bernstien's primary interest was in the excitable properties of nerve cells rather than cardiac cells. 7 cell's membrane (24) . Cole and Curtis in the 1930's went on to discover how the resistance across a cell membrane changed as cells became excited. ...
... (RV). They found that the highest frequency region corresponded to the 24 Temporally established heterogeneities such as alternans have also been regarded as a mechanism which can contribute to patterns of fibrillatory conduction. 25 Dominant Frequency is another analytical tool used in the investigation of cardiac arrhythmias. ...
... complex behavior of fibrillatory conduction. The predominant explanation for the generation of fibrillatory conduction is that there are inherent structural and electrical heterogeneities24 throughout the heart which disrupt propagation and lead to wavebreak, rotor initiation and an overall destabilization of uniform propagation.A lot of work has been done investigating the effects of structural heterogeneities. However, it has only been recently, with the development of many molecular, genetic and imaging techniques, which much examination of the regional ionic heterogeneities and their role in fibrillation has begun. ...
Spatial dispersion of action potential duration (APD) is a substrate for cardiac fibrillation, but the mechanisms are still poorly understood. Spatial APD dispersion has also been associated with both regional fibrillatory patterns as well as regional ionic heterogeneities in cardiac tissue. In particular, regional gradients in two major repolarizing potassium channels, hERG (IKr) and Kir2.1 (IK1), have been implicated in fibrillation. We investigated the role of spatial APD dispersion and the mechanisms by which regional heterogeneity in hERG and Kir2.1 expression contribute to fibrillation. Using a structurally uniform experimental model, neonatal rat ventricular myocyte monolayers, and a novel regional magnetofection technique, we were able to isolate the effects of regional ion channel heterogeneity on electrical propagation. In combination with computer simulations, we were able to provide crucial insights into the underlying mechanisms of arrhythmias.
Regional hERG overexpression shortened APD and increased rotor incidence in the infected region. It also generated fibrillatory conduction in a frequency- and location-dependent manner. The APD gradient only generated wavebreak if activity was faster than 12.9 Hz and originated within the infected region. Simulations determined that hERG-induced transient hyperpolarization is an important factor in rotor frequency but is not significant for the generation of wavebreak. In contrast, Kir2.1 overexpression generates both APD shortening as well as a stable
hyperpolarization of the resting membrane potential. Regional Kir2.1 heterogeneity results in both an APD gradient as well as bimodal spatial and frequency-dependent conduction velocity (CV) gradient. Simulations reveal the bimodal CV gradient to be the result of the balance of sodium channel availability and potassium conductance. Regional Kir2.1 overexpression generated fibrillatory conduction in a frequency and location dependent manner. However, the minimal frequency required for wavebreak was only 10.8 Hz; this suggests that tissue containing Kir2.1 gradients may be more susceptible to fibrillation than tissue containing hERG gradients. This study provides insight, at the molecular level, into the mechanisms by which both spatial APD and bimodal CV dispersion contribute to wavebreak, rotor stabilization and fibrillatory conduction.
... Prompted by this finding, Bernstein set out to measure the complete time-course of the nerve impulse with the use of a differential rheotome, a devise he invented and which allowed precise recordings of very fast electrical processes. Besides describing the kinetics of the negative Schwankung, he also estimated that at rest the nerve interior was about 60 mV more negative compared to the surface (De Palma and Pareti, 2011;Piccolino, 1998). Also around this time, another landmark discovery was made when Cajal, later called "the father of modern neuroscience", reported that the nervous system consisted of discrete individual cells, which would afterwards be known as neurons. ...
Nerve impulse generation and propagation are often thought of as solely electrical events. The prevalence of this view is the result of long and intense study of nerve impulses in electrophysiology culminating in the introduction of the Hodgkin-Huxley model of the action potential in the 1950s. To this day, this model forms the physiological foundation for a broad area of neuroscientific research. However, the Hodgkin-Huxley model cannot account for non-electrical phenomena that accompany nerve impulse propagation, for which there is nevertheless ample evidence. This raises the question whether the Hodgkin-Huxley model is a complete model of the nerve impulse. Several alternative models have been proposed that do take into account non-electrical aspects of the nerve impulse and emphasize their importance in gaining a more complete understanding of the nature of the nerve impulse. In our opinion, these models deserve more attention in neuroscientific research, since, together with the Hodgkin-Huxley model, they will help in addressing and solving a number of questions in basic and applied neuroscience which thus far have remained outside our grasp. Here we provide a historico-scientific overview of the developments that have led to the current conception of the action potential as an electrical phenomenon, discuss some major objections against this conception, and suggest a number of scientific factors which have likely contributed to the enduring success of the Hodgkin-Huxley model and should be taken into consideration whilst contemplating the formulation of a more extensive and complete conception of the nerve impulse.
... Like many major advances in science, Bernstein's membrane theory relied upon a previous set of developments in a different but related field, in this case, physical chemistry (De Palma & Pareti, 2011). These developments began with the theory of solution osmotic pressure derived by Jacobus Henricus van't Hoff (1852e1911), a Dutch chemist and recipient of the first Nobel Prize in Chemistry (1901). ...
This review glances at the voltage-gated sodium (Na⁺) channel (NaV) from the skewed perspective of natural history and the history of ideas. Beginning with the earliest natural philosophers, the objective of biological science and physiology was to understand the basis of life and discover its intimate secrets. The idea that the living state of matter differs from inanimate matter by an incorporeal spirit or mystical force was central to vitalism, a doctrine based on ancient beliefs that persisted until the last century. Experimental electrophysiology played a major role in the abandonment of vitalism by elucidating physiochemical mechanisms that explained the electrical excitability of muscle and nerve. Indeed, as a principal biomolecule underlying membrane excitability, the NaV channel may be considered as the physical analog or surrogate for the vital spirit once presumed to animate higher forms of life. NaV also epitomizes the "other secret of life" and functions as a quantal transistor element of biological intelligence. Subplots of this incredible but true story run the gamut from electric fish to electromagnetism, invention of the battery, venomous animals, neurotoxins, channelopathies, arrhythmia, anesthesia, astrobiology, etc.
... Arrhenius contacted Von't Hoff in a personal communication and put him on the track to explain the observed anomalies based on the dissociation hypothesis. Eventually, Nernst, who was studying the relationship between electricity and electrolyte movements, developed Von't Hoff's equations for the calculation of the electric potential and electromotive force in galvanic cells [79,80]. ...
All modern cells are bounded by cell membranes best described by the fluid mosaic model. This statement is so widely accepted by biologists that little attention is generally given to the theoretical importance of cell membranes in describing the cell. This has not always been the case. When the Cell Theory was first formulated in the XIXth century, almost nothing was known about the cell membranes. It was not until well into the XXth century that the existence of the plasma membrane was broadly accepted and, even then, the fluid mosaic model did not prevail until the 1970s. How were the cell boundaries considered between the articulation of the Cell Theory around 1839 and the formulation of the fluid mosaic model that has described the cell membranes since 1972? In this review I will summarize the major historical discoveries and theories that tackled the existence and structure of membranes and I will analyze how these theories impacted the understanding of the cell. Apart from its purely historical relevance, this account can provide a starting point for considering the theoretical significance of membranes to the definition of the cell and could have implications for research on early life.
Reviewers
This article was reviewed by Dr. Étienne Joly, Dr. Eugene V. Koonin and Dr. Armen Mulkidjanian.
In the tradition of Galvani and Aldini, Carlo Matteucci used a newly developed galvanometer to record a current flow between the cut and intact surface of a frog nerve or muscle that he called the demarcation current. The cut surface had a negative potential relative to the intact surface. Emil du Bois-Reymond identified the electrical event associated with nerve excitation of muscle that he called the negative variation, later known as the action potential. Herman Helmholtz measured the speed of the action potential as it moved down the nerve to the muscle and it was surprisingly slow (about 30 m/s) compared to the speed of electricity moving along a wire. His student Julius Bernstein showed that the action potential lasted about 1 ms and its time course was independent of the stimulus strength. The debate over localized versus generalized function of the cerebral cortex was convincingly resolved by clinical–pathological studies in patients and electrical stimulation of the brain in primates. Functions were clearly localized within the cerebral cortex. Finally, Charles Sherrington used electrical stimulation of the spinal cord to study the integrative function of the nervous system. He introduced the concept of a synapse and showed how complex behaviors such as walking and scratching could still occur in a rudimentary form after the spinal cord had been resected from the brain.
Based on Walther Nernst’s equation describing the potential difference between two salt solutions of different concentrations separated by a semipermeable membrane, Julius Bernstein developed his theory of cell membrane polarization at the turn of the twentieth century. The negative electrical potential inside excitable nerve and muscle cells was due to selective permeability of the cell membrane to potassium ions. Bernstein speculated that during an action potential, there was a brief reversible breakdown in the selective permeability allowing potassium ions to enter the cell. Keith Lucas and Edgar Adrian demonstrated the “all-or-nothing principle” of nerve transmission and suggested that the action potential moved down the nerve by exciting the nerve region just ahead enough to propagate the signal. Development of thermionic vacuum tubes for rectifying and amplifying electronic signals along with improved electrometers allowed researchers to accurately record action potentials for the first time. By taking advantage of the giant squid axon that could be penetrated with a glass electrode and a new voltage-clamp technique, Allan Hodgkin and Andre Huxley determined that the action potential resulted from independent changes in permeability for sodium and potassium ions with the conductance changing as a function of time and membrane potential. They went on to develop a mathematical model based on opening and closing of ion channels in the axon membrane that provided a remarkably accurate prediction of the threshold, shape, and propagation of the action potential. Finally, the patch-clamp technique allowed investigators to measure the current in a single ion channel.
Proteins are the workhorses of cells, performing most of the important functions which allow cells to use nutrients and grow, communicate among each other, and importantly, die if aberrant behavior is detected. How were proteins discovered? What is their role in cells? How do dysfunctional proteins give rise to cancers? Landmark Experiments in Protein Science explores the manner in which the inner workings of cells were elucidated, with a special emphasis on the role of proteins. Experiments are discussed in a manner as to understand what questions were being asked that prompted the experiments and what technical challenges were faced in the process; and results are presented and discussed using primary data and graphs.
Key Features:
- Describes landmark experiments in cell biology and biochemistry.
- Discusses the "How" and "Why" of historically important experiments.
- Includes primary, original data and graphs.
- Emphasizes biological techniques, that help understand how many of the experiments performed were possible.
- Documents, chronologically, how each result fed into the next experiments.
Research devoted to characterizing phenomena is underappreciated in philosophical accounts of scientific inquiry. This paper develops a diachronic analysis of research over 100 years that led to the recognition of two related electrophysiological phenomena, the membrane potential and the action potential. A diachronic perspective allows for reconciliation of two threads in philosophical discussions of phenomena—Hacking’s treatment of phenomena as manifest in laboratory settings and Bogen and Woodward’s construal of phenomena as regularities in the world. The diachronic analysis also reveals the epistemic tasks that contribute to establishing phenomena, including the development of appropriate investigative techniques and concepts for characterizing them.
This article focuses on approaches to link transcriptomic, proteomic, and peptidomic datasets mined from brain tissue to the original locations within the brain that they are derived from using digital atlas mapping techniques. We use, as an example, the transcriptomic, proteomic and peptidomic analyses conducted in the mammalian hypothalamus. Following a brief historical overview, we highlight studies that have mined biochemical and molecular information from the hypothalamus and then lay out a strategy for how these data can be linked spatially to the mapped locations in a canonical brain atlas where the data come from, thereby allowing researchers to integrate these data with other datasets across multiple scales. A key methodology that enables atlas-based mapping of extracted datasets—laser-capture microdissection—is discussed in detail, with a view of how this technology is a bridge between systems biology and systems neuroscience.
The epithelial cells of the gastrointestinal (GI) tract communicate with each other and with cells of other organs via a complex network of highly regulated movement of ions and biomolecules. The molecules ensure regulated activity of cells, tissues, and organs of the GI system and the body as whole. The regulated movement and subsequent activities of the biomolecules released from one cell to the target are made possible by receptive substances (receptors) localized on the membrane of the target cells or intracellular organelles, or in the cytosol. This process, which is referred to as cell-to-cell communication or cellular signaling, ensures the regulated functioning of the cells and tissues of the GI system and the whole organism. This chapter is dedicated to the mechanism of cell-to-cell communication and signaling in normal and relates it to how disease develops. Basic mechanisms of GI epithelial cell signaling and gut nutrient receptor sensing (GI chemosensation) are discussed.
Argument
This paper arrives at a normative position regarding the relevance of Henri Bergson's philosophy to historical enquiry. It does so via experimental historical analysis of the adaptation of cinematographic devices to physiological investigation. Bergson's philosophy accorded well with a mode of physiological psychology in which claims relating to mental and physiological existence interacted. Notably however, cinematograph-centered experimentation by British physiologists including Charles Scott Sherrington, as well as German-trained psychologists such as Hugo Münsterberg and Max Wertheimer, contributed to a cordoning-off of psychological from physiological questioning during the early twentieth century. Bergson invested in a mode of intellectual practice in which psychological claims had direct relevance to the interpretation of physiological nature. The in-part cinematograph-inspired breakdown of this mode had significance for subsequent interpretations of his philosophy. It is suggested that this experimental particularization of Bergson's contentions indicates that any adaptation of his thought for historical enquiry must be disciplinarily specific.
This book looks at how three kinds of strongly electric fishes literally became "electrical," and how they helped to change the sciences and medicine. These fishes are the flat torpedo rays common to the Mediterranean, the electric catfishes of Africa, and an "eel" from South America. The discovery of the electrical nature of these fishes in the second half of the 18th century was the starting point of the two fundamental advances in the sciences: on the physiological side, the demonstration that nerve conduction and muscle excitation are electrical phenomena; and on the physical side, the invention of the electric battery. Starting with catfish tomb drawings from Ancient Egypt and colorful descriptions of torpedoes from the Classical Era, the chapters in this book show how these fishes were both fascinating and mysterious to the ancients. After all, not only could they produce torpor and temporary numbness when touched, they could stun through intermediaries, such as wet nets and spears. Various explanations were given for these remarkable actions in ancient times, including the idea that they might release some sort of cold venom. Through the Renaissance, they also tended to be associated with occult and magical qualities. During the 1600s, natural philosophers speculated that rapid movements of specialized muscles could account for their actions. This idea was widely accepted until the 1750s, when the possibility that their shocks might be electrical began to be discussed. Showing how researchers set forth to provide support for fish electricity is a major focus of this book. Here the chapters transport us into the jungles of South America and later show how some live eels were transported to London, where John Walsh demonstrated in 1776 that they can actually spark. Subsequent chapters deal with further evidence for specialized fish electricity and how electric fishes helped to change ideas about even our own physiology. The book also shows how these fish remained a part of medicine, and how Volta modeled his revolutionary "pile" or electric battery on their anatomy.
This book examines the history of Western attempts to explain how messages might be sent from the sense organs to the brain and from the brain to the muscles. It focuses on a construct called animal spirit, which would permeate philosophy and guide physiology and medicine for over two millennia. The book's story opens along the Eastern Mediterranean, where it examines how Pre-Socratic philosophers related the soul to air-wind or pneuma. It then traces what Hippocrates, Plato, and Aristotle wrote about this pneuma, and how Stoic and Epicurean philosophers approached it. It also visits Alexandria, where Hellenistic anatomists provided new thoughts about the nerves and the ventricles. Thereafter the book shows how Galen's pneuma psychikon or spiritus animae would provide an explanation for sensations and movements. Galen's writings would guide science and medicine for well over a thousand years, albeit with some modifications. One change, found in early Christian writers Nemesius and Augustine, involved assigning perception, cognition, and memory to different spirit-filled ventricles. The book then turns to how questions began to be raised about it in the 1500s and 1600s. Here it examines the rise of modern science. Nevertheless, the animal spirit doctrine continued to survive because no adequate replacement for it was immediately forthcoming. The replacement theory stemmed from experiments on electric fishes started in the 1750s. Additional research eventually led scientists to abandon their time-honored ideas. The book traces some of the developments leading to modern electrophysiology and ends with an epilogue centered on what this history teaches us about paradigmatic changes in the life sciences.
This article examines the science of electrophysiology developed by Emil du Bois-Reymond in Berlin in the 1840s. In it I recount his major findings, the most significant being his proof of the electrical nature of nerve signals. Du Bois-Reymond also went on to detect this same ‘negative variation’, or action current, in live human subjects. In 1850 he travelled to Paris to defend this startling claim. The essay concludes with a discussion of why his demonstration failed to convince his hosts at the French Academy of Sciences.
La science ne consiste pas en faits , mais dans les conséquences que l'on en tire. Claude Bernard, Introduction à l'étude de la médicine expérimentale
Good talkers are only found in Paris.François Villon, Des Femmes de Paris
This essay recounts a controversy between a pioneer electrophysiologist, Emil du Bois-Reymond (1818-1896), and his student, Ludimar Hermann (1838-1914). Du Bois-Reymond proposed a molecular explanation for the slight electrical currents that he detected in frog muscles and nerves. Hermann argued that du Bois-Reymond's 'resting currents' were an artifact of injury to living tissue. He contested du Bois-Reymond's molecular model, explaining his teacher's observations as electricity produced by chemical decomposition. History has painted Hermann as the wrong party in this dispute. I seek to set the record straight.
Preceded by a companion paper on Galvani's life, this article is written on the occasion of the bicentenary of the death of Luigi Galvani. From his studies on the effects of electricity on frogs, the scientist of Bologna derived the hypothesis that animal tissues are endowed with an intrinsic electricity that is involved in fundamental physiological processes such as nerve conduction and muscle contraction. Galvani's work swept away from life sciences mysterious fluids and elusive entities like "animal spirits" and led to the foundation of a new science, electrophysiology. Two centuries of research work have demonstrated how insightful was Galvani's conception of animal electricity. Nevertheless, the scholar of Bologna is still largely misrepresented in the history of science, because the importance of his researches seems to be limited to the fact that they opened the paths to the studies of the physicist Alessandro Volta, which culminated in 1800 with the invention of the electric battery. Volta strongly opposed Galvani's theories on animal electricity. The matter of the scientific controversy between Galvani and Volta is examined here in the light of two centuries of electrophysiological studies leading to the modern understanding of electrical excitability in nerve and muscle. By surveying the work of scientists such as Nobili, Matteucci, du Bois-Reymond, von Helmholtz, Bernstein, Hermann, Lucas, Adrian, Hodgkin, Huxley, and Katz, the real matter of the debate raised by Galvani's discoveries is here reconsidered. In addition, a revolutionary phase of the 18th century science that opened the way for the development of modern neurosciences is reevaluated.
This short review recollects the many essential milestones in electrophysiology that were published in Pflügers Archiv. These involve the first measurement of an action potential by J. Bernstein, the requirement of Na+ for the generation of excitation, the prediction of a lipoid membrane surrounding cells by E. Overton, the physical explanation of the resting membrane potential by J. Bernstein, the first detailed description of the conductance properties of excitable tissues by L. Hermann, and more recently the publication of the patch-clamp method by E. Neher and B. Sakmann.
Julius Bernstein belonged to the Berlin school of "organic physicists" who played a prominent role in creating modern physiology and biophysics during the second half of the nineteenth century. He trained under du Bois-Reymond in Berlin, worked with von Helmholtz in Heidelberg, and finally became Professor of Physiology at the University of Halle. Nowadays his name is primarily associated with two discoveries: (1) The first accurate description of the action potential in 1868. He developed a new instrument, a differential rheotome (= current slicer) that allowed him to resolve the exact time course of electrical activity in nerve and muscle and to measure its conduction velocity. (2) His 'Membrane Theory of Electrical Potentials' in biological cells and tissues. This theory, published by Bernstein in 1902, provided the first plausible physico-chemical model of bioelectric events; its fundamental concepts remain valid to this day. Bernstein pursued an intense and long-range program of research in which he achieved a new level of precision and refinement by formulating quantitative theories supported by exact measurements. The innovative design and application of his electromechanical instruments were milestones in the development of biomedical engineering techniques. His seminal work prepared the ground for hypotheses and experiments on the conduction of the nervous impulse and ultimately the transmission of information in the nervous system. Shortly after his retirement, Bernstein (1912) summarized his electrophysiological work and extended his theoretical concepts in a book Elektrobiologie that became a classic in its field. The Bernstein Centers for Computational Neuroscience recently established at several universities in Germany were named to honor the person and his work.
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