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Birth of the Sliding Filament Model of Muscular Contraction: Proposal

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Mechanism of Muscular Contraction

Part of the book series: Perspectives in Physiology ((PHYSIOL))

Abstract

The official date of the “birth” of the sliding filament theory of muscular contraction is May 22, 1954. On this day the journal Nature published two papers consecutively under the general title: “Structural Changes in Muscle During Contraction”. The first paper by Andrew F. Huxley and Dr. Rolf Niedergerke was entitled: “Interference microscopy of living muscle fibres”. The second paper by Dr. Hugh Huxley and Dr. Jean Hanson was entitled: “Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation”. But the story of sliding filaments begins before May 22, 1954. In order to understand and appreciate the experiments that were done and why they were done, it is necessary to review the scientific background of each of the investigators.

…it is postulated that stretching of the muscle takes place, not by an extension of the filaments, but by a process in which the two sets of filaments slide past each other…one may note the possibility that an analogous process is involved in contraction.

Hugh E. Huxley (1953b)

Koscak Maruyama remembers Jean Hanson shouting: “I know I cannot explain the mechanism yet, but the sliding is a fact” (Maruyama 1995. With permission Oxford University Press)

K. Maruyama (1995)

The motion pictures taken by A. Huxley of living muscle can leave little doubt in the spectator’s mind about the basic correctness of the theory. (Szent-Gyorgyi 1960. With permission Elsevier)

A. Szent-Gyorgyi (1960)

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Notes

  1. 1.

    Andrew Huxley did not work for a Ph.D. at Trinity College in Cambridge and thus he is the only one of the four authors on the classic 1954 papers who is not listed as “Dr.”. During his time at Trinity promising young researchers would receive a research fellowship. Alan Hodgkin (1977) also did not work for a Ph.D.

  2. 2.

    Andrew Huxley is a member of the famous Huxley family. His grandfather was Thomas Henry Huxley, the well known nineteenth century biologist who was Charles Darwin’s “bulldog” (see footnote #4, Chap. 1). Andrew Huxley’s half-brothers were the famous writer Aldous Huxley (1894–1963), author of the book Brave New World, and evolutionary biologist Julian Huxley (1887–1975), the first Director General of United Nations Educational, Scientific and Cultural Organization (UNESCO). For a biography on the Huxley family, see Clark (1968).

  3. 3.

    The Nobel Prize in Physiology or Medicine in 1963 was awarded jointly to John Carew Eccles, Alan Lloyd Hodgkin and Andrew Fielding Huxley “for their discoveries concerning the ionic mechanisms involved in excitation and inhibition in the peripheral and central portions of the nerve cell membrane”. Hodgkin and Huxley did not work with Eccles, an Australian scientist, who investigated the physiology of synapses (Eccles 1964). Hodgkin (1992) has described the “near-miss” of the Nobel Prize in 1962 and the ceremony in 1963.

  4. 4.

    The Nobel Prize in Chemistry in 1962 was awarded jointly to Max Ferdinand Perutz (1914–2002) and John Cowdery Kendrew (1917–1997) “for their studies of the structures of globular proteins”. Perutz solved the so-called phase problem and this solution proved to be the breakthrough that opened up the whole field of protein crystallography. Perutz elucidated the 3D structure of hemoglobin and Kendrew the 3D structure of myoglobin. The Nobel Prize in Physiology or Medicine in 1962 was awarded jointly to Francis Harry Compton Crick (1916–2004), James Dewey Watson (b. 1928) and Maurice Hugh Frederick Wilkins (1916–2004) “for their discoveries concerning the molecular structure of nucleic acids and its significance for information transfer in living material”. They discovered the famous double helix of DNA. See Watson’s (1968) entertaining account of the race to the double helix.

  5. 5.

    The X-ray diffraction pattern is recorded in reciprocal space which means that reflections farther from the origin (wide angle reflections) are due to repeating structures that are close together and reflections near the origin (low or small angle reflections) are due to repeating structures that are further apart.

  6. 6.

    Phase contrast microscopy. There is little absorption of light rays passing through living cells and thus they are essentially transparent. The cells do contain constituents that exhibit small differences in refractive index. These inclusions do not affect the amplitudes of the light rays but do cause the light waves to differ in phase according to the path that they have taken through the cell. The image formed by such rays consists of a pattern of phase differences of uniform brightness, and as such is essentially invisible. Frederick Zernike, of Groningen, produced a visible image in these circumstances by deliberately advancing or retarding the main beam, after it traversed the specimen, by one-quarter of a wavelength, without disturbing the diffracted rays. Consequently, when the whole beam was reunited, conditions for interference existed, and the transparent specimen produced an image where refractive index differences are now observed as differences in transparency. Thus changes in phase became changes in intensity. Zernike received the Noble Prize for this discovery in 1953. For more information on phase contrast microscopy, see Slayter (1976).

  7. 7.

    Hugh Huxley noted (1953b) that the differences in spacings of the elements in the hexagonal array as observed in the X-ray pattern (450 Å) of living muscle isolated from frogs and in the electron micrographs (200–300 Å) must be indicative of shrinkage of the tissue in preparation for electron microscopy.

  8. 8.

    The gating current was not actually detected until the 1973 by C. M. Armstrong and F. Bezanilla in sodium channels of the squid giant axon and by M. F. Schneider and W. K. Chandler (1973) in frog skeletal muscle excitation-contraction coupling.

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  1. Department of Physiology and Cell Biology, Ohio State University, Columbus, OH, USA

    Jack A. Rall

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Rall, J.A. (2014). Birth of the Sliding Filament Model of Muscular Contraction: Proposal. In: Mechanism of Muscular Contraction. Perspectives in Physiology. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2007-5_2

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