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Historical Perspective: Centenary Series: 2 |
1 Department of Physiology, Dartmouth Medical School, Dartmouth-Hitchcock Medical Center, Lebanon, NH 03756, USA
(Received 10 September 2007;
accepted after revision 13 September 2007; first published online 14 January 2008)
Corresponding author W. M. St-John: Department of Physiology, Dartmouth Medical School, Dartmouth-Hitchcock Medical Center, Lebanon, NH 03756, USA. Email: walter.m.stjohn{at}dartmouth.edu
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The control of contraction of muscles in multiple organs, under both normal conditions and in disease, was a primary focus of Professor Buchthal's research activities. Commencing in 1929, these research activities spanned 47 years, with a total of three hundred and seven publications. While such a career is exceptional both in longevity and productivity, the career of Fritz Buchthal is truly extraordinary in that it included two periods of forced exile from his native Germany and, later, another period of exile from his adopted Denmark. During the first period, commencing in 1926, Buchthal managed to gain admission to Stanford University in California while holding a full-time series of labour jobs. At Stanford, he worked in the laboratory of the Nobelist J. J. R. MacLeon, who first interested him in the physiology of muscle. After returning to Germany, Buchthal completed his medical studies and commenced his experimental career at the Kaiser Wilhelm Institute in Berlin. With the rise of Nazism, he was summarily deprived of this position, but was able to find another in Denmark. This residency was short lived because the prosecution of European Jewry spread to Denmark late in the War, forcing Buchthal into exile in Sweden. Fortunately, after the War, the rest of Buchthal's career was marked by tranquility and achievement. A long and distinguished research and administrative career in Denmark was followed, upon ‘retirement’, by positions in the United States, first at the National Institutes of Health and later at various institutions in California.
Electromyography was a technique that Professor Buchthal had used extensively for at least a decade prior to its adaptation by Dr Faaborg-Anderson to investigation activities of the intrinsic muscles of the larynx. Interestingly, as Professor Buchthal notes, their studies were not the first recordings of activities of the intrinsic muscles of the larynx. In 1944, Weddell and colleagues at Oxford obtained such recordings in a number of patients having various diseases and/or injuries. While Weddell et al. (1944) did not study the relationship between laryngeal activity and vocalization, they did note the relationship between this laryngeal activity and respiration, with the larynx opening during inspiration and closing in expiration.
The studies of laryngeal electromyography reported in 1959 had been undertaken to evaluate the role of contraction of laryngeal muscles in phonation (Buchthal, 1959). For many years, a ‘myloelastic theory’ for phonation had been accepted. This ‘passive’ theory held that sound was produced by air pressure acting against the transversely oscillating vocal cord. In the first of a number of illustrative analogies, Professor Buchthal likens this method of production of sound to ‘lips pressed against the mouthpiece of a trumpet.’ A newer ‘active’ theory proposed that sound resulted from oscillatory movements of the vocal cords, as determined by activities of the laryngeal nerves and muscles.
Professor Buchthal appears to have been a member of the age of physiologists for whom experimentation was driven by logic and thought, rather than by technology. The ‘active theory’ for phonation, in its purest form, would require that action potentials of laryngeal nerves and muscles be generated at a range of frequencies from 60 to 1000 s–1. Professor Buchthal reports that such frequencies would be necessary to account for the ‘more than four octaves from the bass tone at 60 per second of a Don Cossack to the soprano's note of more than 1000 per second in the Magic Flute.’ Such high frequencies are above the maxima that can be generated by nerve or muscle. Hence, even before experimentation, logic had established that the frequency of sound production could not correlate directly with the frequency of contraction of laryngeal muscles.
Experimental studies consisted of the somewhat heroic procedure of inserting needle electrodes into a number of intrinsic muscles of the larynx (Faaborg-Andersen & Buchthal, 1956; Faaborg-Andersen, 1957). However, Professor Buchthal notes that Dr Faaborg-Andersen had achieved ‘great skill in the procedure which he accomplishes with only slight discomfort to the subject, as I personally can witness.’ One has the strong suspicion that both investigators were experimental subjects for their own studies.
Before analysing changes in activities of laryngeal muscles with phonation, the correlation of these activities with laryngeal abduction and adduction was noted, as was the relationship with breathing. Contrary to what was expected, the closure of the larynx during expiration was found to be largely passive, with little activity of adductor muscles. Opening during inspiration was the active component, due activity of the posterior cricoarytenoid muscle. These changes of laryngeal diameter and activities during the respiratory cycle have been confirmed in many subsequent publications (see Bartlett, 1986 for review).
As opposed to activity during spontaneous breathing, activities of laryngeal adductor muscles all increased and that of abductor muscles declined during phonation. With their system, Faaborg-Andersen and Buchthal were able to record activities of single motor units in some trials. The frequency of these single action potentials did not increase with an increase in volume of sound but did increase markedly with an increase in pitch, but only to a maximum of 20–50 s–1, which is well below the maximal frequency of sound produced. Other interesting observations of their study were that the electromyographic activity of the laryngeal muscles increased several hundred milliseconds before the production of sound and the change in activity occurred with the ‘thought of vocalization’, even if no sound was produced.
Thus, in summary, Buchthal concluded that phonation was the result of both ‘active’ neurophysiological and ‘passive’ mechanical processes. Stated differently, vocalization results in the vocal cords being pushed apart by increased subglottal pressure. The increased subglottal pressure is a function of contraction of ‘respiratory muscles’ of the chest wall and abdomen. The position and movements of the vocal cords, defined by activities of laryngeal nerves, defines the pitch and quality of sound (Bouhuys et al. 1966; Hillel, 2001; Sataloff et al. 2004).
These studies of Faaborg-Andersen and Buchthal were to remain as the definitive work linking laryngeal function and phonation until Hillel published his comprehensive evaluation of laryngeal electromyography in 2001. While confirming this earlier work, Hillel massively expanded knowledge of laryngeal function by recording simultaneously activities of eight laryngeal muscles in humans. Based upon these findings, Hillel (2001) used electromyography to evaluate laryngeal function in a number of patients with various types of laryngeal dysfunctions (see also Sataloff et al. 2004).
Use of electromyography to evaluate human disease was the primary focus of Fritz Buchthal's work in the final decades of his scientific life, with the review ‘Electromyography in the evaluation of muscle diseases’ being published in 1985 (Buchthal, 1985). Also continuing throughout these later years was his association with and training of junior colleagues in this field of clinical electromyography.
References
Bartlett D (1986). Upper airway motor systems. In Handbook of Physiology, section 3, The Respiratory System, vol. II, Control of Breathing, part 1, ed. Cherniack NS & Widdicombe JG, pp. 223–245. American Physiological Society, Bethesda, MD, USA.
Bouhuys A, Proctor DF & Mead J (1966). Kinetic aspects of singing. J Appl Physiol 21, 483–496.
Buchthal F (1959). Electromyography of intrinsic laryngeal muscles. Q J Exp Physiol Cogn Med Sci 44, 137–148.
Buchthal F (1985). Electromyography in the evaluation of muscle diseases. Neurol Clin 3, 573–598.[Medline]
Faaborg-Andersen K (1957). Electromyographic investigation of intrinsic laryngeal muscles in humans. Acta Physiol Scand 41 (Suppl. 140), 1–149.[Medline]
Faaborg-Andersen K & Buchthal F (1956). Action potentials from internal laryngeal muscles during phonation. Nature 177, 340–341.[CrossRef][Medline]
Hillel AD (2001). The study of laryngeal muscle activity in normal human subjects and in patients with laryngeal dystonia using multiple fine-wire electromyography. Laryngoscope 111 (Suppl. 97), 1–47.[Medline]
Payan J (2004). Fritz Buchthal. Br Med J 328, 1322.
Sataloff RT, Mandel S, Mann EA & Ludlow CL (2004). Practice parameter: laryngeal electromyography (an evidence-based review). J Voice 18, 261–274.[CrossRef][Medline]
Weddell G, Feinstein B & Pattle RE (1944). The electrical activity of voluntary muscle in man under normal and pathological conditions. Brain 67, 178–257.
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