Significance of mechanoreceptors in the subglottal mucosa for subglottal pressure control in singers

Significance of mechanoreceptors in the subglottal mucosa for subglottal pressure control in singers

Journal of Voice Vol. 9, No. 1, pp. 20-26 © 1995 Raven Press, Ltd., New York Significance of Mechanoreceptors in the Subglottal Mucosa for Subglotta...

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Journal of Voice

Vol. 9, No. 1, pp. 20-26 © 1995 Raven Press, Ltd., New York

Significance of Mechanoreceptors in the Subglottal Mucosa for Subglottal Pressure Control in Singers Johan Sundberg, Jenny Iwarsson, and Ann-Marie Holm Billstr6m Department of Speech Commtmication and Music Acoustics, KTH, Stockholm, Sweden

Summary: According to Wyke and Kirchner (Wyke B, Kirchner J. Neurology of the larynx. In: Hinchcliffe R, Harrison D, eds. Scientific foundation of otolaryngology. London: William Heinemann Medical Books, 1976:546--66) mechanoreceptors in the subglottal mucosa play a significant role in the control of laryngeal muscle activity in response to changes of subglottal pressure during phonation. In singers this pressure is adapted not only to phonatory loudness but also to fundamental frequency. By spraying Xylocaine solution with a needle inserted into the trachea through the anterior gap between the cricoid and thyroid cartilages, the subglottal mucosa was anesthetized in three singers. The effects on subglottal pressure and fundamental frequency of this anesthesia were examined. The pressure effects varied between the subjects, whereas the fundamental frequency accuracy was adversely affected in all three subjects. The implications of these findings are discussed. Key Words: Singing-Subglottal pressure--Mechanoreceptors--Subglottal mucosa--Anesthesia.

Singers change subglottal pressure within wide ranges because this pressure is varied not only for the purpose of increasing or decreasing vocal loudness, but also with voice fundamental frequency; obviously both loudness and pitch change within wide limits. This has been observed by Rubin et al. (1), Leanderson et al. (2), and others. Because subglottal pressure affects pitch, it can be postulated that failures to match an intended target pressure cause the singer to sing out of tune. In neutral speech, on the other hand, subglottal pressure remains basically constant, except for the typical fall at the end of breath groups (3). This implies that the

sensory system involved in the control of subglottal pressure must be particularly relevant in singers. According to Wyke and Kirchner (4), mechanoreceptors in the subglottal mucosa contribute to the reflex control of the intrinsic laryngeal muscles during phonation. In particular, in a discussion, Wyke (5) claimed that "Topical anesthesia of the subglottal laryngeal mucosa (by injection through the cricothyroid m e m b r a n e ) . . , renders s i n g i n g . . , almost impossible because of lack of accurate pitch and loudness control." "What comes out in terms of pitch from moment to moment during singing is something over which they have no control." Gould and Okamura (6) attempted to inhibit or diminish the activity of the mucosal receptors by means of topical anesthesia applied through the mouth in one male adult speaker. They observed that during anesthesia the subject used higher subglottal pressures in loud phonation. Also, they found that the time delay between the onset of activity in some breathing muscles and the onset of phonation tended to increase slightly during anes-

Accepted January II, 1994. Address correspondence and reprint requests to Dr. J. Sundberg at Department of Speech Communication and Music Acoustics, KTH, Box 70014, S-10044 Stockholm, Sweden. This investigation was first presented at the 22nd Annual Symposium Care of the Professional Voice, Philadephia, Pennsylvania, June 1993. The work was carried out as a thesis by coauthors J.I. and A.-M.H.B. in Iogopedics at the Department of Phoniattics and Logopedics of the Karolinska Institute, Huddinge Hospital.

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M E C H A N O R E C E P T O R S I N THE SUBGLOTTAL MUCOSA

thesia. The authors concluded that there is a close relationship between voice control and the subglottai reflex system. Garrett and Luschei (7) studied the effect of externally imposed fluctuations of the subglottic pressure on the electromyographic activity in laryngeal muscles during evoked phonation in anesthetized cats. Phonation was evoked by brain stimulation. Somewhat surprisingly, they found "no evidence for reflex discharge of laryngeal muscles that was correlated with subglottic pressure variations produced during evoked phonation." The purpose of the present study was to investigate the relevance of the subglottal mucosal mechanoreceptors to the control of subglottal pressure and fundamental frequency in singers by anesthetizing these receptors. METHOD The anesthesia was administered by a phoniatrician. First, a spot on the skin on the throat was anesthetized with Xylocaine adrenalin, 10 mg/ml. Then a needle was inserted through the cricothyroid ligament at its midline (Fig. I) so that the subglottal mucosa could be sprayed with an anesthetic agent, which was Xylocaine adrenalin 40 mg/ml. The spraying was done during vocal-fold adduction, so as to limit the anesthesia to the subglottal area. The quantity varied between 1 and 4 ml depending on the subjective effect, the criterion for sufficient anesthesia being that the subject felt a pronounced sensation of anesthesia. Because subglottal pressure varies with fundamental frequency in trained singers, an exercise was selected that covered a wide pitch range (Fig.

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2). The singers repeated this sequence 20 times before and 20 times after anesthesia with two [pa:] syllables on each tone. The pitch was decided such that the entire sequence comfortably fitted their personal ranges. A reference pitch was given to the subjects by means of a synthesizer two times, once before and once after the administration of the anesthesia. While singing, the subjects held a thin plastic 5-mm diameter tube, which was connected to a pressure transducer (Glottal Enterprises) in the corner of the mouth. The device was calibrated by means of a manometer. In this way the subgiottal pressure could be estimated as the oral pressure during the [p] occlusion. The output from the pressure transducer, including a set of calibration signals, was recorded together with various other signals on a multitrack FM tape recorder, as illustrated in the block scheme in Fig. 3. The output from an accelerometer (Phonema), fastened to the subject's neck by means of an elastic ribbon, was LP filtered and fed to a pitch tracker (Phonema, double peak-picking system), the output of which, being proportional to the fundamental frequency, was recorded on track. The audio signal as picked up by a SONY microphone was recorded on another track. Three experienced singers volunteered as subjects; two baritones, ages 34 and 56 years, and one alto, age 22 years. The subjects were all interested in voice theory. The subjects sang the triad sequence after they had had a chance to warm up their voices. The pressure signal from the tape recording was analyzed by an oscillograph (Siemens Mingograph) (Fig. 3). The pressures used for the second syllable of each tone in the triad sequence were measured and the mean and the standard deviation across renderings were determined for each tone. Then, the average of all these standard deviations was computed. This mean standard deviation was assumed to reflect how accurately the subject replicated his/her pattern of subglottal pressures when repeating the triad sequence. Therefore, it was used as a measure of the accuracy of the control of subglottal pressure under the various experimental conditions. To check for training effects, the renderings of the triad sequence were grouped into four series, each consisting of 10 renderings; thus there were two series before and two series after anesthesia. Fundamental frequency was measured using the Journal of Voice. Vol. 9. No. 1. 1995

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pa- -pa- -pa- -pa- -pa- -pa-

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FIG. 2. Triad sequence used in the experiment.

SWELL analysis program (8). The fundamental frequency signal was displayed on the computer screen and, excluding onset and decay transients, the signal for each tone was selected for analysis and converted to a frequency histogram (Fig. 4). For technical reasons, the top pitch sung by subject 2 was impossible to measure. The mean of the frequency distribution for each tone was determined. This analysis procedure was applied either directly to the tape-recorded output of the pitch tracker or to the audio signal after pitch tracking, depending on the quality of the recording. The mean fundamental frequency was measured for each individual tone and converted to cent relative to the starting frequency. In this way, it was possible to compare the values of the three subjects in spite of their different pitch ranges. The average across all renderings was then computed for each tone in the triad sequence. The standard deviations of these means were then determined. As with the subglottal pressure, the average of these standard deviations was used as a measure of the accuracy of the control of fundamental frequency under the various experimental conditions. In this way, mean values and standard deviations were obtained for each tone in the triad sequence for every series of 10 repetitions. The mean values

show the average sizes of the intervals sung by each subject in the triad sequence and the standard deviation shows how consistently the subject repeated the pattern. RESULTS Figure 5 shows the subglottal pressures in centimeters H20 as a function of fundamental frequency in semitones relative to the starting frequencies. All subjects increased their subglottal pressure with increasing pitch, as expected. For comparison, corresponding data from subject S I collected from an earlier investigation by Cleveland and Sundberg (9) are also shown in the graph. These data correspond fairly well with our measurements, although the subject consistently used higher pressures and, thus, apparently sang somewhat louder during the present experiment. As mentioned, Gould and Okamura (6) found that under conditions of loud phonation a topical anesthesia of the larynx caused their subject to use higher subgiottal pressures than without anesthesia. Their interpretation was that the anesthesia raised the activation threshold of the mucosal receptors. We observed a similar effect in subject 2 and with regard to the highest pressures also for subject 1,

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Journal of Voice, Vol. 9, No. I, 1995

FIG. 3. Block diagram of the experimental setup. The audio signal was recorded both on a digital audio tape (DAT) recorder and on the TEAC multichannel FM tape recorder. The signal from the accelerometer, fastened to the neck by an elastic ribbon, was amplified, Iowpass filtered, and was used for tracking fundamental frequency. The signal from the pressure transducer captured the oral pressure. During the experiment it was checked together with the fundamental frequency signal of an oscilloscope. Both these signals plus the audio signal were simultaneously recorded on an oscillograph.

MECHANORECEPTORS IN THE SUBGLOTTAL MUCOSA

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FIG. 4. Illustration of the computer method used for measuring fundamental frequency. The upper graph shows the fundamental frequency curve as measured by the SWELL program from the FM tape recorder. The marked section of the third tone was submitted to a histogram analysis, the result of which is shown in the lower graph. The mean fundamental frequency is shown at the top of the histogram.

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whereas for subject 3 no such effect was observed (Fig. 6). Figure 7 illustrates how close to pure the subjects sang. The graph shows the fundamental frequency data for the three subjects as related to the values according to the equally tempered tuning. The deviations from the equally tempered tuning varied between subjects but were smaller than 50 cents in all cases. There was no clear dependence on pitch except for Subject 3 under unanesthetized conditions. Figure 8 shows the effects of anesthesia on the pressure data. The results varied greatly between

the subjects. Subject I exhibited a clear increase of the average standard deviation after anesthesia. The difference between the overall averages for the nonanesthetized to anesthetized conditions clearly exceeded the 95% confidence interval. This indicates that the anesthesia adversely affected the accuracy of his pressure control system. Subject 2, on the other hand, revealed a paradoxical effect: The accuracy of pressure control improved after anesthesia. The decrease of the overall average for the nonanesthetized to anesthetized conditions clearly exceeded the 95% confidence interval. This probably reflected a training effect, the average standard Journal of Voice. Vol. 9, No. 1, 1995

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J. S U N D B E R G E T A L . SUBJECT3, NORMAL

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FIG. 5. Mean subglonal pressures in centimeters H,_O plotted as a function of the fundamental frequency in semitones (st) above the starting frequencies used by the subjects for the different tones in the triad sequence when performed without and with anesthetization of the subglottal mucosa. The lines join data points from adjacent tones in the exercise. The dashes represent the mean -+SD. For subject 1 no data was obtained for the po pitch. The triangles in the leftmost panel show corresponding data previously observed by Cleveland and Sundberg for the same subject (9).

deviation decreasing continuously over her four seties. This subject had not practiced this triad sequence before. The values of subject 3 showed a very slight increase after anesthesia, yet, the difference between the averages for the nonanesthetized to anesthetized conditions exceeded the 95% confidence interval. Figure 9 shows the corresponding results for the fundamental frequencies. Here, the change from nonanesthetized to anesthetized conditions was associated with a deterioration of the fundamental frequency accuracy in all three subjects. Subject 3 showed this deterioration most clearly, while the variations within both conditions were considerable in subject 1. Subject 2 showed a continuous decrease of accuracy throughout the experiment. In spite of these great variations, the difference between the averages for the nonanesthetized and anesthetized conditions clearly exceeded the 95%

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confidence interval for each subject. Thus, it seems fair to conclude that the accuracy of pitch control deteriorated under conditions of anesthesia. DISCUSSION The main purpose of the anesthesia was to affect the mechanoreceptors in the subglottal mucosa. This goal was certainly achieved. Even though the applied amount of anesthetizing agent differed between the subjects, all subjects felt that they became efficiently anesthetized during the experiment. Note also that subject 3, who received the least amount of anesthesia, exhibited the greatest effect on the fundamental frequency control. However, it was impossible to limit the anesthesia to the subglottal mucosa; the subjects' breathing and coughing caused the anesthesia to scatter to the glottal region also. This might be the reason for the 30

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FIG. 6. Averagedsubglottal pressure differencesfor the various tones in the triad sequencebeforeand after anesthesia of the subglottal mucosa. Journal of Voice, Vol. 9, No. I, 1995

M E C H A N O R E C E P T O R S I N THE SUBGLOTTAL MUCOSA

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FIG. 7. The three subjects' mean deviations from the equally tempered tuning when singing the triad sequence 20 times in succession with (solid curves) and without (dash curves) anesthesia of the subglottal mucosa.

observed deterioration of the pitch control. Incidentally, none of the singers found that their capacity to sing was seriously impaired by the anesthesia. In this respect, our observations did not support Wyke's claim that singing became almost impossible during anesthesia of the subglottal region. The effects of anesthesia on subglottal pressure varied between the subjects as shown in Fig. 8. Indeed, each of our three subjects showed a different pattern. Although the training effect prevailed for subject 2, a clear effect was observed for subject 1, whereas the effect was almost nil for subject 3. One possible interpretation is that the different subjects applied different control strategies for subglottal pressure variation; although the mechanoreceptors may have played an important role in subject 1, they were perhaps not used in the control systems of subjects 2 and 3. The subglottal mucosal mechanoreceptors are obviously not the sole feedback generators in the subglottal pressure control sys-

tem. For example,, the lower respiratory tract is provided with mucosal receptors. In any event, the subglottal mucosal mechanoreceptors seem to be of no paramount relevance to the control of subglottal pressure in singers. The variability in fundamental frequency was rather large; under unanesthetized conditions, the frequencies of the tones in the exercise had a standard deviation of 26, 23, and 43 cents, i.e., up to almost half of a semitone. This is far beyond the differential threshold of - 5 cents for musical intervals (10). Also, the frequency averages across trials for the three singers (unanesthetized) showed an average deviation from the equally tempered tuning of 24, 14, and 21 cents, respectively. The greatest mean deviation for a single tone was no less than 50 cents in one of the subjects. Ternstr6m and Sundberg (1 l) found a standard deviation of 13 cents for the fundamental frequencies produced by the members of the bass section of an ambitious amateur so

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FIG. 8. Averaged standard deviations for the subglottal pressures used for the different tones in the four experimental series, each of which consisted of l0 repetitions sung in succession; the first two series were sung without and the last two with anesthesia of the subglottal mucosa.

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FIG. 9. Averaged standard deviations for the fundamental frequency of the different tones in the four experimental series, each of which consisted of l0 repetitions sung in succession; the first two series were sung without and the last two with anesthesia of the subglottal mucosa. Journal of Voice, Vol. 9, No. 1, 1995

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J. S U N D B E R G E T AL.

choir. Taking into consideration that this value was observed when the singers were singing together, most of our values do not seem exceedingly high. A good musical ear is generally considered a mandatory prerequisite for a successful singer. This is certainly true, but it is interesting that our singer subjects clearly sang more out of tune with anesthesia than without, even though the musical ear could hardly have been affected. As mentioned, we assume that this was an effect of a deteriorated proprioception in the glottal region. CONCLUSIONS

The subglottal mucosal mechanoreceptors seem to be of no paramount relevance to the control of subglottal pressure in singers. Anesthesia of the subglottal mucosa impaired the accuracy of fundamental frequency control, presumably because the anesthesia also included the glottal region and, hence, affected proprioception of relevance to pitch control. None of the singers found that their capacity to sing was practically destroyed by the anesthesia. Acknowledgment: We thank Patricia Gramming, M.D., Department of Phoniatrics, Karolinska Hospital, for administering the anesthesia, and Sten Ternstr6m, D. Sc., Department of Speech Communication and Music Acoustics, KTH, for assisting in the measurements. This work was supported by the Swedish Research Council for Engineering Sciences.

Journal of Voice, Vol. 9, No. I, 1995

REFERENCES 1. Rubin H, LeCover M, Vennard W. Vocal intensity, subglottic pressure and airflow relationships in singers. Folia Phoniatr (Basel) 1967;19:393--413. 2. Leanderson R, Sundberg J, von Euler C. Role of diaphragmatic activity during singing: a study of transdiaphragmatic pressures. J Appl Physiol 1987;62:259-70. 3. Lieberman P. Direct comparison of subglottal and esophageal pressure during speech. JAcoust Soc Am 1968;43:115764. 4. Wyke B, Kirchner J. Neurology of the larynx. In: Hinchcliffe R, Harrison D, eds. Scientific foundation ofotolaryngology. London: William Heinemann Medical Books, 1976: 546-66. 5. Wyke B. Discussion of a session paper. In: Titze I, Scherer R, eds. Vocal fold physiology. Biomechanics, acoustics, and phonatory control. Denver: The Denver Center for the Performing Arts, 1985:140. 6. Gould W, Okamura H. Interrelationships between voice and laryngeal mucosal reflexes. In: Wyke B, ed. Ventilatory and phonatory control systems. Oxford: Oxford University Press, 1974:347-59. 7. Garrett J, Luschei E. Subglottic pressure modulation during evoked phonation in the anesthetized cat. In: Baer T, Sasaki C, Harris K, eds. Laryngeal fitnction in phonation and respiration. San Diego, California: Singular Publishing Group, 1991 : 139-53. 8. TernstrOm S. Sound swell manual. Solna, Sweden: Sound Swell, 1991. 9. Cleveland T, Sundberg J. Acoustic analysis of three male voices of different quality. In: Askenfelt A, Felicetti S, Jansson E, Sundberg J, eds. Proceedings of the Stockholm Music Acoustics Conference 1983 (SMAC 83). Stockholm: Royal Swedish Academy of Music Publishers, 46:2, 1985: 143-56.

10. Sundberg J. In tune or not? In: Dahlhaus C, Krause M, eds. Tiefenstruktur der Musik, Festschrift fiir Fritz Winckel. Berlin: Technische Universit~it, 1982:69-97. I 1. Ternstrrm S, Sundberg J. Intonation precision of choir singers. J Acottst Soc Am 1988;84:59--69.