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Why Joseph Erlanger Rejected the Local Circuit Theory of Nerve Impulse Propagation

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Why Joseph Erlanger Rejected the Local Circuit Theory of Nerve Impulse Propagation Why Joseph Erlanger Rejected the Local Circuit Theory of Nerve Impulse Propagation Greg Gandenberger University of Pittsburgh, Department of History and Philosophy of Science 1017 Cathedral of Learning, Pittsburgh, PA 15260. [email protected] Abstract In the 1920s and 1930s, Joseph Erlanger and his colleagues expressed doubts about the local circuit theory of nerve impulse propagation in some of their publications. In 1934, their scepticism inspired Alan Hodgkin to begin a series of experiments that are generally regarded as providing strong support for the local circuit theory. Hodgkin’s experiments are well known, but the nature and sources of Erlanger’s scepticism are not. In the mid-1920s, Erlanger believed that oscillograph recordings indicated that the eddy currents generated by action currents are too small to propagate the nerve impulse as the local circuit theory proposes. In the 1930s, his fundamental objection to the local circuit theory was his belief that eddy currents large enough to propagate nerve impulses would dissipate a large amount of energy and produce uncontrolled stray effects. However, a 1936 discovery led him to admit that eddy currents do at least increase the excitability of an active fiber ahead of the action current wave. His opposition to the local circuit theory diminished further as a result of several developments between late 1938 and early 1939, including most notably Hodgkin demonstration that the resistance of the medium outside the active nerve affects propagation velocity. Word Count: 7467 Keywords Joseph Erlanger; Alan Hodgkin; local circuit theory; membrane theory; St. Louis School; electrophysiology 1. Introduction Early in his 1934-1935 year as a Cambridge undergraduate, Alan Hodgkin discovered that a blocked nerve impulse increases the excitability of the nerve beyond the block. He realized that it would be easy to explain this increase in excitability as the effect of eddy currents flowing ahead of the propagated action current in accordance with the local circuit theory of nerve impulse propagation (Hodgkin, 1976, pp. 3-4). Later in that school year he realized while reading the papers of the “St. Louis School” that many leading physiologists were, as he put it, “thoroughly sceptical both of the membrane theory in general and of the local circuit theory in particular” (Hodgkin, p. 4). Spurred on by their doubts, he decided to investigate whether the increase in excitability beyond a block was in fact an electrical effect as the local circuit theory suggested. Key experiments Hodgkin performed during his investigation of the local circuit theory are now regarded as classics in the history of physiology.1 However, little is known about the views of the St. Louis School that lay behind the expressions of scepticism that helped inspired 1 The most notable of these experiments are presented in Hodgkin (1937a), (1937b), (1939). These experiments are often cited in elementary physiology textbooks, such as Aidley (1998), pp. 46-47. Hodgkin’s work. This paper begins to address that gap by discussing Joseph Erlanger’s views about the local circuit theory. Erlanger was the senior member of the St. Louis School. Hodgkin quotes his objections to the local circuit theory in his autobiography (Hodgkin, 1994, pp. 74-75), but those objections are difficult to understand without more historical context than Hodgkin provides. For instance, Hodgkin quotes Erlanger’s claim that the local circuit theory seemed to him “teleologically…queer” (Hodgkin, p. 74; the original quote is from Erlanger, J., 1910-1965, Erlanger to Hodgkin, January 6, 1937). This statement and others like it that Erlanger made around the same time are quite important for understanding Erlanger’s opposition to the local circuit theory, but they are rather obscure by themselves. An examination of both published and unpublished writings by Erlanger and his colleagues reveals that Erlanger had two fundamental objections to the local circuit theory. First, he believed that the eddy currents flowing in front of an action current wave are too small to re- excite the nerve fiber. Second, he believed that if eddy currents were large enough to re-excite the nerve fiber, then they would produce substantial current leaks away from the active fiber, dissipating energy and producing stray effects. The first objection crystallized between 1924 and 1926, while the second manifested itself between 1932 and 1936. This second objection underlay Erlanger’s claim that the local circuit theory is problematic teleologically. Erlanger’s opposition to the local circuit theory diminished between 1936 and 1939. The details of exactly how and when Erlanger’s opinions changed are not entirely clear from the available documents, but some broad conclusions can be drawn. Erlanger did not argue against the local circuit theory after his January 6, 1937 letter to Hodgkin, either in print or in any of his correspondence that I have examined. However, Hodgkin reported that Erlanger was still “very sceptical” of the local circuit theory when Hodgkin visited Erlanger in St. Louis in April 1938 (Hodgkin, 1994, p. 113). Soon after that meeting Hodgkin met a challenge Erlanger had posed to show that changing the resistance outside the active fiber changes its conduction velocity. It seems that even after he learned about that result, Erlanger continued to entertain the possibility that chemical as well as electrical processes are involved in propagating nerve impulses. However, he no longer questioned that claim that eddy currents are essential to that process. This paper is organized as follows. §2 concerns the period between 1924 and 1926, during which Erlanger argued privately that oscillograph records indicate that eddy currents are too small to be responsible for propagation. §3 concerns the objections to the local circuit theory that Erlanger presented between 1932 and 1936, which were based on the assumption that propagation by eddy currents would be messy and inefficient. §4 concerns the decline of Erlanger’s opposition to the local circuit theory that took place between 1936 and 1939. 2. Erlanger’s first objection: eddy currents are too small to account for propagation (1924- 1926) In 1922, Erlanger and his colleague Herbert Gasser introduced the cathode-ray oscillograph into electrophysiology (Erlanger & Gasser, 1922). George Bishop was brought on as a collaborator in 1923 (Bishop, 1965, p. 1), when Gasser went to Europe for a two-year research leave (Gasser, 1964, p. 10). Their oscillograph could follow the rapid voltage changes that occur during a nerve impulse with far greater fidelity than previous recording techniques. Among other contributions, it promised to provide evidence relevant to the local circuit theory by revealing the size of the eddy currents that flow ahead of the action current wave. However, Erlanger, Gasser, and Bishop disagreed among themselves about the size of the “foot” their action current records contained. That is, they disagreed about how much of their action current records should be attributed to eddy currents rather than to the action current proper. Erlanger and Gasser believed that the foot was negligible, which led them to doubt the local circuit theory. Bishop maintained that the foot was large enough that its size did not provide a strong objection to the local circuit theory. The theoretical context within which this debate took place extends back into nineteenth century. The local circuit theory has its roots in the “Strömchen theory” Ludimar Hermann proposed in the 1872 edition of his Grundriss der Physiologie des Menschen (pp. 323-324; see also Hermann, 1879, pp. 193-194). In that work, Hermann pointed out that the travelling wave of electronegativity associated with the nerve impulse should cause eddy currents to flow into the excited region from neighboring unexcited regions. Such currents would repolarize the excited region and depolarize the unexcited regions. They would thereby tend to restore the excited region to its resting state while exciting the neighboring regions. Hermann proposed that the nerve impulse could propagate itself electrically in this way. Hermann combined this electrical theory of nerve impulse propagation with a chemical theory of the impulse itself (e.g. Hermann, 1867). In the early twentieth century, Bernstein developed the “membrane theory” as an alternative account of the nerve impulse (e.g. Bernstein 1902, 1912). According to the membrane theory, chemical transformations do not play a central role in the nerve impulse. The electrical phenomena associated with the nerve impulse arise from the separation of already existing ions across the nerve’s semipermeable membrane, and the electrical changes during activity arise from a partial breakdown of that membrane. Erlanger, Gasser, and Bishop were influenced by Ralph Lillie (see e.g. Gasser 1924, p. 117; Erlanger & Bishop, 1926, p. 631), who accepted many of the central claims of the membrane theory but argued that the theory was inadequate in the form in which Bernstein presented it (Lillie, 1923, pp. 302-303). Lillie accepted that the demarcation current between injured and uninjured nerve surfaces arises from the separation of ions across the semipermeable membrane and that the membrane at least partially breaks down during activity. However, he argued that Bernstein neglects metabolic processes involved in maintaining the cell membrane and in repairing it after breakdown. He claimed that the chemical composition of the cell membrane changes as a result of these processes and that those changes in membrane composition manifest themselves electrically along with changes in ion concentration (Lillie, p. 311). Lillie also attributed propagation to “local bio-electric circuits” like those postulated by Hermann (Lillie, pp. 322-323, 379-410). The local circuit theory requires that eddy currents extend far enough ahead of the nerve impulse at high enough intensity to be able to produce excitation at a given point ahead of the action current wave in the time it takes the wave to reach that point. Lillie claimed that eddy currents extend three centimeters in advance of the action current wave front at an intensity sufficient to excite (Lillie, p.
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