Vocal Warm-up Increases Phonation Threshold Pressure in Soprano Singers at High Pitch

Vocal Warm-up Increases Phonation Threshold Pressure in Soprano Singers at High Pitch

Vocal Warm-up Increases Phonation Threshold Pressure in Soprano Singers at High Pitch Tamara Motel, Kimberly V. Fisher and Ciara Leydon Evanston, Illi...

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Vocal Warm-up Increases Phonation Threshold Pressure in Soprano Singers at High Pitch Tamara Motel, Kimberly V. Fisher and Ciara Leydon Evanston, Illinois

Summary: Vocal warm-up is thought to optimize singing performance. We compared effects of short-term, submaximal, vocal warm-up exercise with those of vocal rest on the soprano voice (n ⫽ 10, ages 19–21 years). Dependent variables were the minimum subglottic air pressure required for vocal fold oscillation to occur (phonation threshold pressure, Pth), and the maximum and minimum phonation fundamental frequency. Warm-up increased Pth for high pitch phonation (p ⫽ 0.033), but not for comfortable (p ⫽ 0.297) or low (p ⫽ 0.087) pitch phonation. No significant difference in the maximum phonation frequency (p ⫽ 0.193) or minimum frequency (p ⫽ 0.222) was observed. An elevated Pth at controlled high pitch, but an unchanging maximum and minimum frequency production suggests that short-term vocal exercise may increase the viscosity of the vocal fold and thus serve to stabilize the high voice. Key Words: Larynx—Singing—Voice therapy—Voice disorders—Exercise.

INTRODUCTION

instrument” (p. 39). Comparison of pre-exercise and post-exercise voice range profiles, however, did not reveal a reliable physiologic correlate of the perceived benefit. Although vocal warm-up is a routine element in most singers’ regimens, there has been surprisingly little research to define the phonatory effects of short-term, sub-maximal vocal exercise. Only two published studies have demonstrated phonatory benefits of long-term vocal exercise (increased glottal efficiency and high pitch range) when exercise was employed twice daily over a period of four weeks.6 Vocal warm-up is also a component of vocal hygiene and therapy programs,7–9 yet no scientific evidence is available to support its use. In this study, we aimed to show whether or how the high-pitch singing voice may benefit from shortterm, submaximal exercise in the form of a vocal warm-up. Although singing warm-up may alter central processes like attention, memory, and mental preparedness for artistic performance, some physiologic

Vocal warm-up is thought to be prerequisite for optimal singing.1–4 Elliot et al5 tested the proposed benefit of a 30-minute warm-up exercise in singers. Their subjects reported that after warm-up, “it was easier to sing, particularly at high pitches, and that the voice appeared as a more obedient

Accepted for publication May 16, 2002. Presented at the 30th Annual Symposium: Care of the Professional Voice, Philadelphia, Pennsylvania, June 14, 2001. From the Department of Communication Sciences and Disorders, Northwestern University, Evanston, Illinois. Address correspondence and reprint requests to Kimberly V. Fisher, Department of Communication Sciences and Disorders, Northwestern University, 2299 N. Campus Dr., Evanston, IL 60208. E-mail: [email protected] Journal of Voice, Vol. 17, No. 2, pp. 160–167 쑕 2003 The Voice Foundation 0892-1997/2003 $30.00⫹0 doi:10.1016/S0892-1997(03)00003-1

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VOCAL WARM-UP IN SINGERS changes may affect the vocal fold’s muscular body or mucosal cover directly. In skeletal muscle, submaximal exercise redistributes ions and water in blood and muscle.10 In as little as 10 minutes of submaximal exercise, water begins to move from blood plasma11 into interstitial and intracellular spaces.12,13 Sjogaard et al12 reported a 41% increase in extracellular muscle water content and a 2% increase in intracellular water content of the vastus lateralis after submaximal knee extension. More substantial effects were shown for maximal exercise, and those effects began to reverse in as little as 3 minutes of rest. Thus, one can expect that striated muscle will accumulate water after submaximal exercise, an effect that is temporally linked to the performance of that exercise. It is likely that much of this water is protein bound, as exercise-induced hemoconcentration is accompanied by reduction of globulin proteins in the vascular space.11 The exercise-induced water flux into striated muscle has been attributed to increases in muscle contraction and arterial blood flow that amplify capillary hydrostatic pressure. This pressure moves plasma ultrafiltrate into spaces outside vascular tissue.10,14 Working muscle also accumulates metabolic products such as lactate.15 These metabolites increase the osmotic pressure of muscle tissue, encouraging water to flow from vascular tissue into muscle tissue. It is unclear whether similar changes would occur in laryngeal muscle after vocal warm-up. If the striated laryngeal and skeletal musculature were similar metabolically, one could hypothesize similar accumulation of metabolites and associated osmotic water flux after a short duration vocal exercise. The increased hydrostatic pressure gradient would also contribute to hydration of laryngeal muscle, as singing is associated with a rise in blood pressure and sympathetic tone. Exercise-induced water efflux from the circulatory volume and into laryngeal muscle would increase the stiffness of laryngeal musculature, thereby shifting the frequency range upward and favoring the production of high pitches. This prediction assumes that the exercise is not performed to exhaustion, wherein a loss of potassium from muscle cells and a failure of excitation– contraction coupling could cause decline in the forcegenerating capacity of the muscles that elevate vocal

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fundamental frequency. The intrinsic laryngeal muscles, however, are relatively fatigue resistant.16,17 Warm-up potentially alters the water environment of vocal fold mucosa as well. Water is a major constituent of the lamina propria. The osmotic pressure of the lamina propria will be determined in large part by its charge density, and thus the relatively stable concentration of charged molecules (like hyauluronan) that are present in the extracellular matrix. These molecules serve to bind water, inflate the matrix, and thus sustain compressive load18,19 as during phonation. Vocal fold oscillation, however, produces shear and compression forces that may temporarily collapse the capillaries, thereby reducing water flux from the capillaries into the mucosa. Reduced water efflux from the circulatory volume into vocal fold mucosa may increase the viscosity of the mucosa. Increases in vocal fold stiffness and viscosity were expected to influence high-pitch singing. Influx of protein-bound water into muscle may increase the stiffness of the laryngeal muscle. Decreased water flux into the mucosa would increase its viscosity, rendering the tissue less free to flow. The minimum subglottic pressure required for small amplitude vocal fold oscillation (phonation threshold pressure, Pth) varies directly with viscosity.20 We thus hypothesized that submaximal vocal exercise in the form of a singing warm-up would increase the maximum and minimum vocal fundamental frequencies, as well as Pth. METHODS Participants Ten women who were soprano singers from Northwestern University’s School of Music (Table 1) volunteered to participate in the study in accordance with a protocol approved by Northwestern University’s Institutional Review Board. All participants were in full health, and they reported normal voice and hearing. All presented with perceptually normal speech and voice on the days of the experiment. The ages of participants ranged from 19 to 21 years (Mean age ⫽ 20.4 years, SD ⫽ 0.699 years). Participants had received an average of 7.3 years of formal instruction in singing (SD ⫽ 2.1 years) and spent an average of 10.3 hours per week singing Journal of Voice, Vol. 17, No. 2, 2003

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TAMARA MOTEL ET AL TABLE 1.

Subject 1 2 3 4 5 6 7 8 9 10

Age (Yrs)

Formal Singing Training (Yrs)

Singing Time Per Week (Hrs)

20 20 21 20 20 21 21 21 21 19

5.0 7.0 9.0 12.0 5.0 5.5 7.0 7.0 8.0 7.5

10 7 12 15 12 11 5 7 10 14

Note: Mean ⫾ SD: 20.4 ⫾ 0.7, 7.3 ⫾ 2.1, 10.3 ⫾ 3.2.

(SD ⫽ 3.2 hours). All participants sang regularly in private lessons, a choir, or other musical group. No participants smoked or took medication other than birth control. Participants were instructed to maintain their customary dietary and sleep habits on the days of the experiment. All participants arrived for the experiment without having prepared for singing and denied any feeling that their voices were already warmed-up or fatigued. All were naı¨ve to the experimental hypotheses. Instrumentation Volume velocity airflow was obtained using a wide bandwidth differential pressure transducer (Glottal Enterprises PTW-1) coupled to the right side of a vented pneumotachograph facemask. Oral pressure was obtained with a low bandwidth pressure transducer (Glottal Enterprises PTL-1) housed on the left side of the facemask. The oral pressure transducer was coupled to a disposable catheter, 1 in long and 1 mm in diameter, placed translabially at a 45⬚ angle. The volume velocity flow and pressure signals from the transducers were amplified (Glottal Enterprises MSIF-2) and then digitized at 20,000 Hz and 200 Hz, respectively, using a MacLab/8s AD converter and a Power Macintosh 7500/100 computer. MacLab/s v3.5 software was used to plot and store the data. Flow and pressure signals were calibrated prior to each day’s data collection. Experimental Protocol A within-subject repeated measures design was used in which every participant was tested two Journal of Voice, Vol. 17, No. 2, 2003

times on each of two mornings. On Day 1, data were collected immediately before (pre) and after a 10-minute vocal warm-up exercise (post). At the same time on Day 2, data were collected immediately before and after a 10-minute period of complete vocal rest. Differences between pre treatment and post treatment condition measures were compared, where the two treatment conditions were vocal warm-up (Day 1) and rest (Day 2). Because Pth is known to vary directly with vocal pitch, target pitches were selected based on each participant’s individual maximum phonatory frequency range prior to warm-up. The method for establishing target pitches was as follows. On Day 1, using an electronic keyboard, participants were coached to glide up to the highest phonatory pitch that they could sustain for one second. This highest pitch was matched with the keyboard to the nearest semitone. Participants then glided downward to the lowest pitch that they could sustain for one second. This lowest pitch was also matched with the keyboard to the nearest semitone. The maximum phonatory pitch range was calculated in semitones based on the lowest and highest musical notes that were sustained for one second. Three target pitches were calculated to the nearest semitone based on the 10%, 20%, and 80% levels of each subject’s maximum phonatory range in semitones. These target pitches (hereafter called low, comfort, and high pitch) were held constant on both days of the experiment. Each participant was trained to execute the phonation threshold task. Phonation threshold pressure was defined for the participants as the minimum subglottic pressure required for small amplitude vocal fold oscillation to begin. Each participant was instructed to “speak very softly” at her comfortable (20%) pitch. She then practiced speaking /p/ repeatedly at a suprathreshold level with a rate of 1.5 syllables per second following a metronome pulse. She next held the facemask snug over her nose and mouth and spoke the /p/ syllable string of seven syllables on a single breath. The participant was cued with the correct pitch and prompted to produce the syllable string with a “smooth and constant flow of air.” Following the suprathreshold practice, each participant practiced the task at a subthreshold level. Finally, the participant practiced the syllable string

VOCAL WARM-UP IN SINGERS at a level between the supra- and sub-threshold levels. She was instructed to speak “as softly as possible without whispering.” The participant and experimenter viewed the glottal volume velocity on a computer monitor. The participant was instructed to make the glottal volume velocity waveform “as small as possible, but not flat.” In this manner, a minimum threshold was identified above which phonation occurred but below which phonation ceased. After the training period, five threshold trials were collected for each pitch condition (comfortable, high, and low). Trials were excluded and repeated if voicing of the stop consonant was detected or if nasal airflow greater than that expected for small mask movements (12 ml/s) was observed. Trials were also excluded and repeated if pressure peaks were unstable or not flat. To collect maximum F0, each participant performed an upward pitch glide on vowel /u/ to sustain her highest pitch for 1 sec, a task repeated three times. To collect minimum F0, each participant performed a downward pitch glide on vowel /u/ to sustain her lowest pitch for 1 sec, a task also repeated three times. To assure that participants were extending their vocal range as far as possible, they were prompted with the keyboard as described previously. The vocal warm-up exercises performed on Day 1 were developed by Karen Brunssen, a professional vocal instructor and Associate Professor in the Music Performance Studies Department at Northwestern University. The warm-up activity closely resembled the protocol participants performed at the beginning of a routine voice lesson. Participants reviewed an audiotape recording of Dr. Brunssen describing and performing the exercises with piano accompaniment. Participants performed the warmup with audiotaped piano accompaniment and with reference, as necessary, to a written sheet of music. The 10-minute warm-up consisted of five exercises: (1) descending stepwise scales spanning one octave on a text of /zi/ in legato style; (2) ascending and descending stepwise scales spanning one fifth using a text of /zi/ in legato style; (3) ascending major triads on a text of /i/ in staccato style; (4) descending, stepwise thirds on a text of /trioioi/ spanning one half-octave; and (5) allegro ascending and descending scales spanning one octave on a text of /vi/. Upon completion of the vocal warm-up, data

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collection for the phonation threshold, maximum and minimum frequency tasks was repeated. On Day 2, the protocol was repeated with a 10-minute period of complete vocal rest replacing the vocal warm-up. After completing the experiment on Day 2, participants were asked to recall the warm-up from Day 1. Participants then rated their perceived degree of warm-up at that time on an equal appearing interval scale of 1–10, where 1 indicated “not warmed-up at all” and 10 indicated “warmed-up enough for performance.” Data Reduction and Analysis The dependent variables were Pth (⫾0.1 cm H2O), and the maximum and minimum vocal fundamental frequencies (⫾4 Hz). Pth was estimated from the oral pressure during bilabial voiceless stop consonants of quietly spoken consonant-vowel-consonant syllable strings as described and validated elsewhere.21–25 From each seven-syllable trial, the five middle /p/ occlusions were selected for analysis. Pairs of adjacent oral pressure peaks were averaged to approximate the subglottic pressures during the four intervening /i/ vowels. The averaging process yielded 20 subglottic pressure values for each pitch and condition (20 pressure values × 3 pitches × 4 conditions). Five percent of the subglottic pressure data files were reanalyzed a second time to calculate re-measure reliability. First and second measures were strongly correlated (r ⫽ 0.99) and yielded an average absolute difference of 0.027 cm H2O, suggesting reliability was adequate for the purposes of this study. Vocal fundamental frequency was calculated as the inverse of the glottal period derived from the volume velocity airflow. The fundamental frequency trajectory for each glide was obtained and displayed by using computer-automated software for glottal cycle analysis (MacLab). A total of 1 sec, quasiperiodic phonations of the highest and lowest fundamental frequency were selected by cursor placement for each of the three high-pitch and three low-pitch trials, respectively. The average of the three highest frequency trials was taken as the maximum fundamental frequency (Max F0). The average of the three lowest mean fundamental frequency trails was taken as the minimum fundamental frequency (Min F0). Five percent of the Max F0 and Min F0 data files Journal of Voice, Vol. 17, No. 2, 2003

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FIGURE 1. Mean Pth differences (⫾SD) for the rest and vocal warm-up treatments at each of three pitch levels (comfortable, low, and high). Positive and negative differences indicate increases and decreases in mean Pth, respectively.

were reanalyzed a second time to calculate remeasure reliability. First and second measures were strongly correlated (r ⫽ 0.99) and yielded an average absolute difference of 9.66 Hz. A mean pre treatment–post treatment difference was computed for each dependent variable for each subject within each condition. This reduced each participant’s data set to a Day 1 warm-up difference and a Day 2 rest difference for each dependent variable. As inequality of variance was observed among the treatment differences, the non-parametric Wilcoxon Signed Rank Test was used to determine if any treatment differences in Pth, Max F0, and Min F0 for warm-up were significantly different from differences due to vocal rest. Participant 10 was excluded from the Pth analysis because her Day 2 estimate of subglottic pressure was found to be invalid. RESULTS Figure 1 compares the mean Pth differences for rest and vocal warm-up at each of the three pitches (comfortable, low, and high). At high pitch, the mean Pth difference was greater for warm-up than rest (N ⫽ 9, z ⫽ ⫺1.836; df: 1,8; p ⫽ 0.033), but not at comfortable pitch (N ⫽ 9; z ⫽ ⫺.533; df: 1,8; p ⫽ 0.297) or at low pitch (N ⫽ 9; z ⫽ ⫺1.362; df: 1,8; p ⫽ 0.087). With warm-up, the positive Pth difference at high pitch was 0.61 ⫾ 0.74 cm H2O, Journal of Voice, Vol. 17, No. 2, 2003

FIGURE 2. Monotonically decreasing mean Pth for three individual participants (S6, S7, S9) in different pitch conditions (comfort or high-pitch, respectively) across the time-ordered measurement periods (Day1 Pre, Day1 Post, Day2 Pre, Day2 Post).

whereas with rest, there was a negative difference of ⫺0.05 ⫾ 0.63 cm H2O. Between-participant variability in Pth (revealed by the standard deviation of the mean) was greatest at high pitch. At high pitch, six of nine participants demonstrated positive differences in Pth with warm-up. Also, six of nine participants demonstrated a negative difference in Pth with the rest condition. In five of these six participants, a negative difference with rest was less than 0.5 cm H2O. To determine whether a practice effect had contributed to the observed negative differences, a chronological analysis of each participant’s four conditions (Day 1 Pre-, Day 1 Post-, Day 2 Pre-, Day 2 Post) was performed. Three of the nine participants (S6, S7, S9) improved their ability to phonate with minimum subglottic pressure as they became more experienced with the task (Figure 2). Note the monotonically decreasing Pth values; a trend that in two participants (S7 and S9) ran counter to the increased Pth for the group after warm-up when tested under the high-pitch condition. The significantly increased Pth effect for high pitch, however, was detected despite the opposing effect of practice in these participants. Differences in the Max F0 (N ⫽ 10; z ⫽ ⫺.866; df : 1,9; p ⫽ 0.193) and Min F0 (N ⫽ 10; z ⫽ ⫺0.764; df : 1,9; p ⫽ 0.222) between warmup and rest conditions were not significant (Figure 3). Six of ten participants had differences of one

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semitone or less after the warm-up. Participant 1, however, extended her maximum pitch by 3.84 semitones and elevated her low pitch by 2.14 semitones, effectively shifting her range upward. Participant 5 lost 3.89 semitones at the low end of her range with the warm-up. Warm-up ratings obtained after the completion of the experiment ranged from 4 to 8 and indicated that all participants felt somewhat warmed-up but not enough for performance. Participant 1 gave the maximum warm-up rating.

DISCUSSION Vocal warm-up is advocated for optimal singing performance.1–4 Here, we have shown that a controlled warm-up exercise significantly increased Pth when participants vocalized at a frequency that was 80% of their pre-exercise range. This finding was observed despite a Pth training effect in three participants that ran counter to the experimental effects. An increase of Pth with warm-up may appear intuitively inconsistent with the subjective impression that after warm-up it is “easier to sing particularly at high pitches.”5 In contrast, our findings indicate that a greater expiratory effort was required for phonation at high pitch after vocal warm-up. Additionally, there were no reliable effects of vocal warm-up for the participants’ Max and Min F0 (viz., mean differences ⬍1 ST). Consistent increases in Pth,, but not in Max F0 and Min F0 production after warmup, suggest that a more substantial physiologic effect occurred in the vocal fold mucosa than in the muscle. For the mucosa, Titze,20 derived an equation that describes the minimum pressure required for small amplitude oscillation: Pth⫽kBcw/T

(1)

where Pth is phonation threshold pressure, k is the transglottal pressure coefficient, B is the mean damping coefficient for mechanical vibration, c is the mucosal wave velocity, w is the prephonatory glottal half-width, and T is the vocal fold thickness (assuming a one-mass model of the vocal folds), and k is a constant (≈1.1). This equation posits a direct relationship between Pth and the tissue damping coefficient (B), a factor directly related to viscosity of

FIGURE 3. Mean semitone differences in minimum (Min) and maximum (Max) vocal pitch for vocal rest and warm-up treatments. Positive and negative differences indicate increases and decreases, respectively.

the mucosa. The increase in Pth with vocal warmup in the present investigation leads one to consider that submaximal vocal exercise possibly increased the viscosity of the mucosa. This increase in viscosity may have resulted from a loss of water from the vocal fold mucosa during warm-up, despite a simultaneous increase in water in the muscle. The vascular supply to the mucosa is anatomically and functionally distinct from that of the muscular vocal fold.26,27 In dogs, vocal fold oscillation induces a transient ischemia in the superior layer of the lamina propria.28 As the endothelium is more permeable when exposed to shear stress, a transient ischemia may be necessary to prevent vascular injury during phonation. Such a transient, oscillation-induced ischemia would decrease the volume of water available to the mucosa, thereby increasing viscosity. It is interesting to consider that an increase in viscosity, when not extreme, may also allow singers to stabilize high vocal pitches more easily, a desirable outcome of vocal warm-up. Detailed understanding of mechanisms that underlie the increased Pth due to a decrease in internal or superficial vocal fold hydration awaits further study. Oral breathing, more common in singing than in rest breathing, reduces the humidity of inspired air and may contribute to superficial drying of the airway mucosa.29,30 The large standard deviations of means of all dependent variables demonstrate individual variability in the effects of the warm-up task. It is likely Journal of Voice, Vol. 17, No. 2, 2003

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that a controlled warm-up task does not provide equal exercise and thus equal warm-up for different individuals. Although each participant had a unique baseline frequency range and singing skill, the warm-up tasks were inflexible in tempo and ascended to a fixed pitch. The level and pattern of muscle activation used by subjects in this study may have varied. Singers with a more restricted upper frequency limit may use a higher level of muscle activation than singers who can easily extend their vocal capabilities beyond the task demands. When a task requires sustained muscle activation that exceeds 40% of maximum voluntary contraction, muscle ischemia can occur.31 To better equate the perceived degree of warm-up among participants, an alternative procedure (albeit less rigorously controlled) could have been employed wherein each participant performed her personalized vocal exercises such that she felt adequately prepared for performance. The subjective rating at the end of this experiment confirmed that not all participants felt equally warmed-up at the end of the exercise. On the 1–10 scale, scores ranged from 4 to 8. Participant 1, who extended her upper range by almost four semitones with the warm-up, reported the subjective rating of 8, indicating nearly performance ready. The lack of significant effect on Max and Min F0 did not confirm the hypothesized increase in muscle or mucosal stiffness with vocal warm-up. We have considered the possibility that the laryngeal muscles are metabolically unlike skeletal muscles in the extremities.32 The larynx may have robust mechanisms for maintaining a consistent fluid environment when the vocal system is put under a stress such as sub-maximal exercise. For example, laryngeal muscles may possess enzymes that transport or process exercise-induced metabolites before they have an opportunity to accumulate in the muscle tissue. Transient ischemia introduced by sustained isometric contraction also might minimize water flux into muscle. In either case, an increase in muscle stiffness would not occur to an appreciable degree and a dramatic upward shift in range of frequency production would not be observed. Some tissue characteristics may also vary across individuals according to genetic influence. To achieve reliable and substantial increases in the upper frequency limit may require an extended program of vocal exercise33 that offers Journal of Voice, Vol. 17, No. 2, 2003

potential for vocal motor learning, as well as changes in muscle fiber type or density to accommodate the characteristics of neural input. Although this study examined phonation threshold pressure and range of frequency production, a study of other phonatory measures could further show how vocal warm-up affects the voice. Measures of vocal stability (perturbation), accuracy, onset, and aerodynamic power or efficiency are just a few possibilities. Such measures might be sensitive to improvements in coordination, mental readiness, or carrying power of the voice. The present investigation, however, demonstrates that short-term vocal exercise in the form of a warm-up can engender physiologic change with potential to enhance vocal performance. Submaximal exercise in the form of a vocal warmup affects phonation in a manner different from that previously supposed. An elevated phonation threshold pressure has long been associated with pathological voice and considered detrimental to vocal performance. Yet six of the nine healthy singers who participated in this study experienced an elevated Pth at high pitch after warm-up. Participants denied that voice worsened after the warm-up. The warm-up also was one used effectively by the students in prior training. These results compel us to reexamine some assumptions about optimal vocal performance. Is lowering phonation threshold pressure always desirable? Perhaps an elevated phonation threshold is a negative trade-off for other more desirable phonatory effects. It is possible that the increased Pth relates to a protective ischemia that prevents vascular injury in the vocal fold mucosa during high frequency phonation. We propose that increased vocal fold viscosity may even stabilize high frequency phonation, making the soprano voice less susceptible to disruption and “a more obedient instrument.”5

Acknowledgements: This work was completed in partial fulfillment of The Honor’s Program in Human Communication Sciences and Disorders at Northwestern University. The authors gratefully acknowledge the assistance of Karen Brunssen and Charles Larson. This project was supported in part by K23 DC00168 from the National Institution of Deafness and Other Communication Disorders.

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Journal of Voice, Vol. 17, No. 2, 2003