10
Journal of Voice Vol. 11, No. 1, pp. 23-32 © 1997Lippincott-RavenPublishers, Philadelphia The Role of Strap Muscles in Phonation Laryngeal Model In Vivo Canine Ki Hwan Hong, *Ming Ye, *Young Mo Kim, *Kevin F. Kevorkian, and *Gerald S. Berke Department of Otolaryngology, Chonbuk National University, Medical School, Chonbuk, Korea; and *Division of Head and Neck Surgery, UCLA School of Medicine, Los Angeles, California, U.S.A. Summary: In spite of the presumed importance of the strap muscles on laryn- geal valving and speech production, there is little research concerning the physiological role and the functional differences among the strap muscles. Generally, the strap muscles have been shown to cause a decrease in the fundamental frequency (Fo) of phonation during contraction. In this study, an in vivo canine laryngeal model was used to show the effects of strap muscles on the laryngeal function by measuring the Fo, subglottic pressure, vocal in- tensity, vocal fold length, cricothyroid distance, and vertical laryngeal move- ment. Results demonstrated that the contraction of sternohyoid and sternothy- roid muscles corresponded to a rise in subglottic pressure, shortened cricothy- roid distance, lengthened vocal fold, and raised Fo and vocal intensity. The thyrohyoid muscle corresponded to lowered subglottic pressure, widened cricothyroid distance, shortened vocal fold, and lowered F0 and vocal inten- sity. We postulate that the mechanism of altering Fo and other variables after stimulation of the strap muscles is due to the effects of laryngotracheal pulling, upward or downward, and laryngotracheal forward bending, by the external forces during strap muscle contraction. Key Words: Strap muscles--Fo - Intensity--Subglottic pressure--Cricothyroid distancewVocal fold length. It is generally agreed that the extrinsic laryngeal muscles are important for laryngeal function in deglutition to lift and tilt the larynx as part of bio- logical valving and phonation (1,2), but their pho- natory function is less well defined. A large number of muscles participate indirectly or directly in the functioning of the larynx, including infrahyoid (strap), suprahyoid, pharyngeal constrictor, and ex- trinsic tongue muscles. These can be divided mainly into two groups: the strap muscles and the supra- hyoid muscles (1). The location of the origin and insertion of the strap muscles are unique for each muscle, implying functional differences among the strap muscles. Accepted May 24, 1996. Address correspondence and reprint requests to Dr. Ki Hwan Hong, Department of Otolaryngology, Chonbuk National Uni- versity, Medical School, Chonju, Chonbuk, 560-180, KOREA. The literature has described several human studies relating the functional role of the strap muscles to the larynx, attributing changes in the length of the vocal folds to external forces such as contraction of the strap muscles (3-7). However, there still re- mains some controversy on the function of these muscle acts. Sonninen (8) stimulated the sternothyroid muscle of a patient under local anesthesia with the neck extended and found lowering of the pitch. Faaborg- Anderson and Sonninen (9) studied laryngeal posi- tion and the electrical activity in the extrinsic laryn- geal muscles during phonation at different pitches. They reported that the electrical activity of ster- nothyroid muscle showed pronounced activity at low pitch and decreased activity at high pitch. In the thyrohyoid and mylohyoid muscles, electrical activity increased at high pitch. Hirano et al. (5) 23

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Page 1: The Role of Strap Muscles in Phonation In Vivo Canine ... Voice... · MA) were applied to the isolated RLNs. A constant current nerve stimulation (WR Medical electronics RLN Stimulator,

Journal of Voice Vol. 11, No. 1, pp. 23-32 © 1997 Lippincott-Raven Publishers, Philadelphia

The Role of Strap Muscles in Phonation Laryngeal Model

In Vivo Canine

Ki Hwan Hong, *Ming Ye, *Young Mo Kim, *Kevin F. Kevorkian, and *Gerald S. Berke

Department of Otolaryngology, Chonbuk National University, Medical School, Chonbuk, Korea; and *Division of Head and Neck Surgery, UCLA School of Medicine, Los Angeles, California, U.S.A.

Summary: In spite of the presumed importance of the strap muscles on laryn- geal valving and speech production, there is little research concerning the physiological role and the functional differences among the strap muscles. Generally, the strap muscles have been shown to cause a decrease in the fundamental frequency (F o) of phonation during contraction. In this study, an in vivo canine laryngeal model was used to show the effects of strap muscles on the laryngeal function by measuring the F o, subglottic pressure, vocal in- tensity, vocal fold length, cricothyroid distance, and vertical laryngeal move- ment. Results demonstrated that the contraction of sternohyoid and sternothy- roid muscles corresponded to a rise in subglottic pressure, shortened cricothy- roid distance, lengthened vocal fold, and raised F o and vocal intensity. The thyrohyoid muscle corresponded to lowered subglottic pressure, widened cricothyroid distance, shortened vocal fold, and lowered F 0 and vocal inten- sity. We postulate that the mechanism of altering F o and other variables after stimulation of the strap muscles is due to the effects of laryngotracheal pulling, upward or downward, and laryngotracheal forward bending, by the external forces during strap muscle contraction. Key Words: Strap muscles--F o - Intensity--Subglottic pressure--Cricothyroid distancewVocal fold length.

It is generally agreed that the extrinsic laryngeal muscles are important for laryngeal function in deglutition to lift and tilt the larynx as part of bio- logical valving and phonation (1,2), but their pho- natory function is less well defined. A large number of muscles participate indirectly or directly in the functioning of the larynx, including infrahyoid (strap), suprahyoid, pharyngeal constrictor, and ex- trinsic tongue muscles. These can be divided mainly into two groups: the strap muscles and the supra- hyoid muscles (1).

The location of the origin and insertion of the strap muscles are unique for each muscle, implying functional differences among the strap muscles.

Accepted May 24, 1996. Address correspondence and reprint requests to Dr. Ki Hwan

Hong, Department of Otolaryngology, Chonbuk National Uni- versity, Medical School, Chonju, Chonbuk, 560-180, KOREA.

The literature has described several human studies relating the functional role of the strap muscles to the larynx, attributing changes in the length of the vocal folds to external forces such as contraction of the strap muscles (3-7). However, there still re- mains some controversy on the function of these muscle acts.

Sonninen (8) stimulated the sternothyroid muscle of a patient under local anesthesia with the neck extended and found lowering of the pitch. Faaborg- Anderson and Sonninen (9) studied laryngeal posi- tion and the electrical activity in the extrinsic laryn- geal muscles during phonation at different pitches. They reported that the electrical activity of ster- nothyroid muscle showed pronounced activity at low pitch and decreased activity at high pitch. In the thyrohyoid and mylohyoid muscles, electrical activity increased at high pitch. Hirano et al. (5)

23

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24 K. H. H O N G ET AL.

reported that greater electrical activity of the ster- nohyoid muscle at lower pitches appears to be re- lated chiefly to the lower position of the larynx, but also the muscular activity increased at higher pitches. Simada and Hirose (10) also reported that a consistent increase in the activity of the sternothy- roid muscle was observed in association with pitch lowering with decreased activity during pitch rise. However, the activity of the sternohyoid muscle showed no consistent correlation with pitch lower- ing. Ohala and Hirose (l l) reported that the sterno- hyoid muscle is active in both lowering the pitch and in achieving extremely high pitch, but in speech the involvement in pitch lowering is most notice- able. Erickson et al. (12,13) reported that the strap muscles have a negative relationship to frequency and a strong negative correlation with the activity of the geniohyoid and cricothyroid muscles. Simada and Hirose (I0) also reported that the sternohyoid muscle helps at least to maintain a low pitch at a low level during an utterence.

There are a few reports that the strap muscles have a positive relation to frequency with stimula- tion of strap muscles resulting in pitch elevation. Sonninen (14) reported that the function of the ex- trinsic laryngeal muscles, the so-called "external frame function," are considered to lengthen or shorten the vocal folds and regulate pitch by chang- ing the relation of the thyroid to the cricoid carti- lage. He argued that simultaneous contractions of sternothyroid muscles resulted in a forward force on the thyroid cartilage tending to increase the ten- sion of the vocal folds. He postulated that section- ing the various external laryngeal muscles would result in lowering the voice, loss of range, and fail- ure of the glottis to close completely. Murakami and Kirchner (15,16) suggested that the external laryn- geal muscles appear to make two contributions to the tensor mechanism of the larynx, shortening of the cricothyroid distance and contraction of the thy- roarytenoid muscle. Niimi et al. (6) supposed that the sternothyroid muscle could serve as a pitch raiser. They speculated that the thyroid cartilage rotates downward around the cricothyroid joint, or the frontal part of the cricoid ring comes closer to the thyroid cartilage and the arytenoid cartilage, which results in higher tension of the vocal folds.

The present study used an in vivo canine laryn- geal model (17,18) to evaluate the effects of strap muscle stimulation on the vocal folds. Stimulation to the sternohyoid, sternothyroid, and thyrohyoid muscles was performed. The frequency (Fo), sub-

glottic pressure (Psub), and vocal intensity were calculated from waveform signals. Vertical laryn- geal movement, cricothyroid distance, and vocal fold length were measured using monitored video images (19,20). The study allowed us to evaluate the role of each individual strap muscle on stimulation and then postulate the mechanism involved in alter- ing pitch.

MATERIALS AND METHODS

In vivo canine model The in vivo canine model of this experiment (Fig.

I) was similar to that used in previous reports (17,18). Four healthy mongrel dogs (-25-30 kg) were premedicated with acepromazine maleate in- tramuscularly. Intravenous pentobarbital sodium (Nembutal) was administered to a level of corneal anesthesia. Additional pentobarbital sodium was used to maintain this level of anesthesia throughout the procedure. Each dog was placed supine on the operating table. Orotracheal intubation was per- formed.

A midline incision was made to expose the strap muscles from the mandible to the sternal notch. The sternohyoid, sternothyroid, and thyrohyoid mus- cles were dissected carefully. The recurrent laryn- geal nerve (RLN) was isolated about 5 cm inferior to the larynx, and bilateral ansa cervicalis nerve branches to the sternohyoid, sternothyroid, and thyrohyoid muscles were dissected leaving l-cm segments. The most active nerve branch to each strap muscle was identified via stimulation. A low tracheotomy was performed at the level of the su- prasternai notch and an endotracheal tube was placed for ventilation. A second tracheotomy was performed in a more superior location and a cuffed endotrachei tube was passed superiorly with the tip positioned about l0 cm below the glottis. For direct visualization of the larynx through the oral cavity, a button was used to suspend the epiglottis.

Nerve stimulation Harvard subminiature electrodes (South Natick,

MA) were applied to the isolated RLNs. A constant current nerve stimulation (WR Medical electronics RLN Stimulator, Model S2LH, St. Paul, MN) was used to provide constant amounts of current to the RLNs equal bilaterally. The frequency of stimula- tion was 80 Hz with a pulse duration of 1.5 milli- second for both nerve stimulators. A Grass model 54H stimulator (Quincy, MA) was used to provide

Journal of Voice, Vol. 11, No. 1, 1997

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THE STRAP MUSCLES 25

video camera

macro lens - - - . ( ~ Y s o u n d \

~ / ~ ¢ meter ~ endoscope ~ level

........ e rve ~¢ n

• ° . .

A A RLN stimulation

pressure transducer

video recorder T V mon i to r

osci l loscope pr in te r

/ image

processing

computer digitization

FIG. 1. Schemat i c p resen ta t ion of in vivo laryngeal model. R L N = recurrent laryngeal nerve; SH = s t e r n o h y o i d m u s c l e ; ST -- s ternothyroid muscle; TH = thy- rohyoid muscle .

varying amounts of current to the isolated nerves of the strap muscles. Voltage varied from 0 to 3 V for strap muscle stimulation, and was classified as low or high levels according to the contraction of strap muscles. Low-level stimulation was the level at which the strap muscles contracted mildly on direct visual observation. Maximal stimulation was deter- mined by lack of additional contraction of the strap muscles. During maximal stimulation of the isolated nerves of the strap muscles, no contraction of the cricothyroid muscle was noted.

Airflow and pressure system Room air was warmed and humidified by bub-

bling through 5 cm of water at 37°C and air flow was controlled by a needle valve (Whitey, Highland Heights, OH) and measured with a flowmeter (model FI500; Gilmont instruments, Great Neck, NY). The rate of air flow was about 400 ml/sec. A Millar catheter-tipped pressure transducer (model SPC-303 Millar Instruments, Houston, TX) was in- serted through the superior tracheotomy to rest 2 cm below the glottis. The transducer was calibrated at the temperature of the animal's trachea by sub- merging it in a water bath at 37°C to a depth just covering the sensor (0.5 cm) and then calibrating it against a mercury manometer from 0 to 100 mmHg.

Waveform signals during phonation The subglottic and acoustic signals were verified

on a Tektronix oscilloscope (model 5116 Beaverton,

OR) before recording. Then the signals were re- corded on a personal computer with a Labmaster analog-to-digital microprocessor. The acoustic waveforms were recorded with subglottic pressure simultaneously and these signals were low-pass fil- tered at 3,000 Hz and digitized at a rate of 20 kHz. A multipurpose computer program (Cspeech 3.1) was used to analyze the subglottic and acoustic sig- nals. The fundamental frequency of each trial was calculated by measuring the vocal period from the subglottic pressure curve.

Measurements of vocal fold length Videoendoscopy was performed using a Storz tel-

escope connected with a fiberoptic cable for mea- suring vocal fold length. Images were recorded us- ing a CCD camera (Toshiba IKC30A, Buffalo Grove, IL) and ¥4-inch videotape recorder (SONY VO-9850, Park Ridge, N J). Recorded video images were viewed on a SONY video monitor (PVM 1341) and images were printed out by a SONY video color printer. The calibration method was used to mea- sure change of vocal fold length before and after stimulation as in Fig. 2. A standard centimeter ruler was lowered to the level of the glottis and measured with the software, so that pixel units could be con- verted to square millimeters (19,20). The camera was kept at a constant distance from the larynx throughout each experiment,

Journal of Voice, Vol. 11, No. 1, 1997

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26 K. H. HONG ET AL.

FIG. 2. Photograph with ruler measuring the vocal fold length between two markers on the vocal fold demonstrating the calibration method.

Measurements of the vertical level of larynx and cricothyroid distance

Downward movements of thyroid and cricoid cartilages were calculated by measuring the vertical lowering of the larynx. Small needles with markers were placed on the midline of the thyroid lamina at the vocal cord level and at the midline of the ante- rior cricoid lamina. Images were recorded using a CCD camera (Toshiba IKC30A) and a 3/4-inch vid- eotape recorder (SONY VO-9850). Recorded video images were viewed on a SONY video monitor (PVM 1341) and images were printed out using a SONY video color printer. Using video images, the extent of vertical laryngeal movements during stim- ulation were calculated by the movement of the needle on the thyroid cartilage while the ruler was constantly adjusted by holding it at the side of the larngotrachea. The changes of cricothyroid distance were measured by the differences in the needle movements on the thyroid and the cricoid cartilages before and after stimulation.

Experimental design Four dogs were studied by varying the stimula-

tion level to the isolated nerves to the strap mus- cles. Low and high levels were employed using con- stant air flow and bilateral RLN stimulation. Three trials were performed for each condition separated by 3 to 5 minutes to reduce fatigue effects. During each trial, the subglottic pressure and acoustic sig-

nals were digitized. Data were evaluated at 300- millisecond intervals. Subglottal pressure, F 0, and vocal intensity were averaged from ten consecutive cycles selected at random from a stable section of phonation. Videoendoscopic images were used to measure the change of vocal fold length. The move- ments of the cricoid and thyroid cartilages were cal- culated from video images of the external thyroid and cricoid cartilage needles.

RESULTS

A two-way analysis of variance (ANOVA) with replication was undertaken for all dependent vari- ables. Stimulation condition (with or without the strap muscle) was a within-subjects factor; dogs, stimulation site, and stimulation level were be- tween-subjects factors. Table I shows the mean changes of all dependent variables for each dog.

For the sternohyoid muscle, Fo, vocal intensity and subglottic pressure showed significant increase after stimulation in F o and subglottic pressure, but not in vocal intensity (see Table 2 and Fig. 3). Sig- nificant interaction occurred between dogs and lev- els of stimulation for dependent variables (F3,16 = 670.3, p < 0.01) and vocal intensity (F3.16 = 10.6, p < 0.05), and subglottic pressure (F3,16 = 26.3, p < 0.01). Some of the dependent measures were moderately correlated using Pearson's correlation adjusted for multiple comparisons (Fo and vocal in-

Journal o f Voice, Vol. II, No. I, 1997

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THE STRAP MUSCLES 27

T A B L E 1. Mean changes of dependent variables with stimulations, a

Dog ! Dog 2 Dog 3 Dog 4 Muscle

variables Low High Low High Low High Low High

SH F o 8.3 27.0 19.5 35.3 25.7 38.3 19.1 76.8 Intensity 0.2 0.3 1.4 0.7 0.5 0.3 0.1 1.3

Psub 8.7 15.8 4.3 6.0 17.1 20.7 9.9 35.6 CTD 0.0 - 2.0 - 1.0 - 2.0 0.0 - 2.0 - 1.0 - 2.0 VFL - 3 . 0 - 7 . 6 - 5 . 3 5.8 0.0 7.4 2.4 8.0 VLM - 2 . 4 - 9 . 5 - 2 . 5 - 11.5 - 2 . 0 - 13.5 - 1.0 - 6 . 0

ST F o 7.8 23.2 10.0 20.6 5.1 16.4 12.7 57.3 Intensity 0.5 1.4 1.6 1.5 0.1 0,2 0.3 0.7 Psub 11.2 12.5 5.6 8.9 1. I 12,6 5.4 9.9 CTD 0.0 - 2 . 0 0.0 - 2 . 0 0.0 - 2 . 0 - 1.0 - 2 . 0 VFL 0.0 5.4 3.0 6.0 - 4 . 3 5.6 - 5 . 7 5.5 VLM - 2.0 - 7.5 - 1.5 - 8.0 - 2.0 - 9.5 - 3.0 - 6.0

TH F o - 3 . 6 - 8 . 1 - 4 . 1 ~7 .4 - 6 , 3 - 10,9 - 3 . 0 - 10.8 Intensity - 0. I - 0.3 - 0.2 - 0.3 - 0.1 0.0 0.0 - 0.2 Psub - 1.4 4.5 - 0 . 9 - 2 . 2 - 0 . 6 - !.6 - 2 . 3 - 5 . 4 CTD 0.0 2.0 1.0 2.0 0.0 2.5 1.0 2.5 VFS 0.0 - 3.8 0.0 - 5.0 0.0 - 6.4 - 3.4 - 5.4 VLM 1.0 3.5 2.0 6.0 0.0 5.5 !.0 8.0

Airflow was held constant at 400 cc/s relatively. SH. sternohyoideus; ST, sternothyroideus; TH, thyrohyoideus; F o, fundamental frequency (Hz); Intensity, acoustic power (volt); Psub, subglottic pressure (mmHg); CTD, cricothyroid distance (ram); VSM, vertical laryngeal movement (mm); VFL, vocal fold length (mm).

tensity: r = .46, p < 0.05; intensity and subglottic pressure: r = 0.16, p > 0.05; F0 and subglottic pres- sure: r = 0.83, p < 0.01).

Vertical laryngeal movement , cricothyroid dis- tance, and vocal fold length for the sternohyoid muscle showed significant difference before and af- ter stimulation and between levels of stimulation as shown in Table 3. The vertical levels of the larynx were lowered and the cricothyroid distances were shortened after stimulation of this muscle. The vo- cal folds were lengthened slightly after low level

stimulation, but significantly increased in the high level stimulation as shown in Fig. 4. Significant in- teraction occurred between dogs and levels of stim- ulation for the dependent variables vocal fold length (F3,16 = 12.7, p < 0.01) and vertical movement (F3,16 = 3.5, p < 0.05), but not for cricothyroid distance (F3,16 = 0.7, p > 0.05). These dependent measures were significantly correlated using Pear- son's correlation between vocal fold length and ver- tical movement (r = 0.779, p < 0.01), but not be- tween vocal fold length and cricothyroid distance (r

T A B L E 2. Overall changes and statistical data fo r F o, vocal intensity, and subglottic pressure after stimulation

Overall changes ANOVA (A) A N O V A (B) Muscle

variables Low High df F P df F P

SH Fo (Hz) 18.2 Intensity (volt) 0.6 Psub (mmHg) 10.0

ST F o (Hz) 8.9 Intensity (volt) 0.6 Psub (mmHg) 5.8

TH F o (Hz) - 4 . 3 Intensity (volt) - 0 . 1 Psub (mmHg) - 1.3

44.3 i,40 71.7 <0.01 1,16 161.8 <0.01 0.7 1,40 42.4 <0.01 i, 16 0.38 >0.05

19.5 1,40 87.2 <0.01 1,16 78.5 <0.01

29.4 1,40 41.7 <0.01 1,16 77.4 <0.01 0.9 1,40 75.5 <0.01 1,16 5.2 <0.05

i !.0 1,40 60.4 <0.01 I, 16 12.8 <0.01

- 9.3 1,40 65.1 <0.01 1,16 14.8 <0.01 - 0.2 1,40 30.5 <0.01 I, 16 11.7 <0.01 - 3.4 1,40 50.6 <0.01 1,16 21.9 <0.01

Airflow was held constant at 400 cc/s relatively. SH, sternohyoideus; ST, sternothyroideus; TH, thyrohyoideus; Psub, subglottic pressure (mmHg). ANOVA (A), between before and after stimulation; ANOVA (B), between the levels of stimulation.

Journal of Voice, Vol. 11, No. 1, 1997

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28 K. H. H O N G ET AL.

50 A

~ . 40

30

~: 2 0

o- 10

" 0

-10

FIG. 3. Plots for the changes of Fo(A), vocal intensity (B), and subglottic pressure (C) with levels of stimulation of the strap mus- cles; SH = sternohyoid muscle; ST = sternothyroid muscle; TH = thyrohyoid muscle.

0

t~ e"

m

I B

0.8

0 . 6

0.4

0.2

0

-0.2

18

20 C

E 10 E 10

5

0 D .

-5

0.59

= -0 .327 , p > 0.05) and between cricothyroid dis- tance and vertical movement (r = 0.372, p > 0.05).

For the sternothyroid muscle, Fo, vocal intensity, and subglottic pressure also showed significant dif- ferences with stimulation (Table 2). A significant interaction occurred between dogs and levels of stimulation (F3,16 = 12.2, p < 0.01), but not for the subgiottic pressure (F3,16 = 1.86, p > 0.05) and intensity (F3,16 = 2.3, p < 0.05). F o and subglottic

low

0.61

low

44

-4.2

-0.09

19

. . . ~ , ,

0 . 9 3

low -1.3 ,,,w,,

-9 .3

..0.2

- 3 . 4

pressure were significantly correlated using Pear- son's correlation adjusted for multiple comparisons (r = 0.58, p < 0.01), but not between Fo and inten- sity (r = 0.06, p > 0.05) and vocal intensity and subglottic pressure (r = 0.1, p > 0.05). Figure 4 depicts overall changes for laryngeal movement (lowered), cricothyroid distance (shortened), and vocal fold length (lengthened) after stimulation of the sternothyroid muscle. The vocal fold length was

T A B L E 3. Overall changes and statistical data for the lalwngeal movement"

Overall changes ANOVA (A) ANOVA (B) Muscle

variables Low High df F P df F P

SH VFL (%) - 1.5 7.2 1,40 38.2 <0.01 I, 16 360.7 <0.01 CTD (ram) - 0.5 - 2.3 1,40 35.8 <0.01 1,16 36.5 <0.01 VLM (mm) - 2 . 0 - 10.1 1,40 7.4 <0.01 1,16 400.8 <0.0t

ST VFL (%) - 1.7 5.6 1,40 52.6 <0.01 1,16 189.8 <0.01 CTD (mm) - 0.3 - 2.0 1,40 20.3 <0.01 I, 16 28.0 <0.01 VLM (mm) - 2.1 - 7.7 1,40 4.5 <0.01 I, 16 417.7 <0.01

TH VFL (%) - 0.8 - 5.2 1,40 33.5 <0.01 I, 16 196.9 <0.01 CTD (mm) 0.5 2.3 1,40 52. I <0.01 I, 16 85.9 <0.01 VLM (mm) 1.0 5.8 1,40 31.4 <0.01 1,16 163.7 <0.01

" Cricothyroid distance and vocal fold length after stimulation. SH, sternohyoideus; ST, sternothyroideus; TH, thyrohyoideus; VFL, vocal fold length; CTD, cricothyroid distance; SLM, vertical laryngeal movement. ANOVA (A), between before and after stimulation; ANOVA (B), between the levels of stimulation.

Journal of Voice, Vol. 11, No. 1, 1997

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THE STRAP MUSCLES 29

E

E

o

3

2

E 1

'- 0

I - 0 -2

10

5

0

-5

-10

-3

lO 8 6 A

4 2

e- 0 _J -2

-4 -6

B

C

A

-2

low -0.5 -0.3

low -1.5 -1.7

0.5

I

-0.8

-10

8.6

-7.7

-2.3

8.1

5.8

-5.4

FIG. 4. Plots for the changes of vertical level of larynx (A), CT distance IB) and vocal fold length

- - q (C) with levels of stimulation of strap muscles; SH = sternohyoid muscle; ST = sternothyroid mus- cle; TH = thyrohyoid muscle.

significantly increased in the high-level stimulation state (Table 3). These variables were significantly correlated adjusted for cricothyroid distance and vertical movement (r = 0.69, p < 0.01), vocal fold length and cricothyroid distance (r = 0.535, p < 0.01), and vocal fold length and vertical movement (r = -0 .666 , p < 0.01).

In contrast , the thyrohyoid muscle showed differ- ent responses compared with the sternohyoid and sternothyroid muscles. The values for all variables were significantly different at the 0.05 level for the comparison of no stimulation versus low (or high) stimulation levels. The F 0, vocal intensity, and sub- glottic pressure were lowered after stimulation (Fig. 4 and Table 2). Vocal fold length was decreased, but cricothyroid distance was increased and the larynx was raised after stimulation of the thyrohyoid mus- cle (Fig. 4 and Table 3). No significant interactions occurred between dogs and levels of stimulation for the dependent variable (F3,16 = 0.543, p > 0.05), vocal intensity (F3,16 = 2.3, p < 0.05), subglottic pressure (F3,16 = 1.4, p > 0.05), vocal fold length (F3,16 = 8.2, p < 0.01), cr icothyroid distance (F3,16 = 3.6, p < 0.05), and vertical movement (F3,16 = 7.6, p < 0.01). The dependent measures were moderately correlated between intensity and

subglottic pressure (r = 0.5, p < 0.05), vocal fold length and cricothyroid distance (r = -0 .853 , p < 0.01), vocal fold length, and vertical movement (r = -0 .759, p < 0.01), and cricothyroid distance and vertical movement (r = 0.835, p < 0.01), but not between Fo and intensity (r = 0.08, p > 0.05) and F0 and subglottic pressure (r = 0.37, p > 0.05).

DISCUSSION

The strap muscles have been cons ide red to lengthen or shorten the vocal folds by changing the relationship of the thyroid cartilage to the cricoid cartilages (14). However , the action of the strap muscles during phonation is controversial and has differed from subject to subject depending on vocal habits or vocal training (9,10). So it is difficult to draw general conclusions from human studies. In this canine study, contraction of the sternohyoid and sternothyroid muscles corresponded to raising the subglottic pressure, F o, and vocal intensity. The sternothyroid muscle corresponded to greater ef- fects on subglottal pressure and F o than the ster- nothyroid muscle. Both muscles produced narrow- ing of the cricothyroid distance and lengthening of the vocal folds according to the level of stimulation.

Journal o f Voice, Vol. II, No. I, 1997

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30 K. H. H O N G ET AL.

The thyrohyoid muscle showed opposite activity from the sternohyoid and sternothyroid muscles; that is, significant decrease in F 0, subglottal pres- sure, and intensity.

In terms of larynx and hyoid position, the con- traction of the sternohyoid and sternothyroid mus- cles pulls the hyoid bone downward and forward, thus lowering the larynx or preventing its elevation. In this study, these muscles produced laryngeal and tracheal backward and downward tilting. The thy- rohyoid muscle made the larynx and hyoid bone raise upward without tilting. The movements of the larynx and trachea by sternohyoid and sternothy- roid muscle contraction have been described as laryngotracheal pulling (14). We observed an addi- tional type of movement of the larynx and trachea, laryngotracheai bending, during stimulation of the sternohyoid and sternothyroid muscles. Thus, we propose that the movement of the laryngotrachea by the external laryngeal muscles can be classified by the laryngotracheal pull, upward and downward, and laryngotracheal bending, forward and back- ward (Fig. 5).

The effect of laryngotracheal downward pull dur- ing sternothyroid contraction has two possible ex- planations. Zenker and Zenker (21) reported that a laryngotracheal downward pull can contribute to lowering F 0 by increasing the cricothyroid distance, and thus changing the longitudinal tension of the vocal folds. But in this canine study, the cricothy- roid distance was decreased and F o increased dur- ing laryngotracheal downward pull. This phenome- non can be explained anatomically. The cricoid car- tilage is relatively fixed to the adjacent connective

tissue when compared with the thyroid cartilage, creating restricted vertical movement of the cricoid cartilage compared with the thyroid cartilage. Dur- ing lowering of the larynx, this results in shortening the cricothyroid distance. During contraction of the sternohyoid and sternothyroid muscle, the cricoid and thyroid cartilages move downward together, but the thyroid cartilage moves more than the cricoid, which results in shortening of the cricothy- roid distance.

Shipp et al. (22) postulated that the F 0 raising might be due to increased vertical tension of the vocal folds caused by high lung volumes accompa- nied by greater laryngotracheal pull. Murakami and Kirchner (15) reported that the external laryngeal muscles tend to stabilize or pull the thyroid carti- lage downward and to pull the cricoid cartilage up- ward. This narrows the anterior midline distance, serves as a counterforce to the contraction of the thyroarytenoid muscle, and thus contributes to ten- sion within the vocal folds. Therefore, the strap muscles may participate in the reflex protection mechanism of the larynx. In this canine study, we could not evalute the effect of vertical tension di- rectly during laryngotracheal downward pull. We could observe, however, that the trachea was di- lated during laryngotracheal downward pull, allow- ing higher air volume in the laryngotrachea, with higher subglottic and tracheal pressures. We can therefore postulate that the increase in frequency and vocal intensity might be due to increased sub- glottic pressure during laryngotracheal pulling or a counterforce to the contraction of the thyroaryte- noid muscle, and thus contribute to tension within

forward ~ f o r w a r d ~ li / t~;';.":~l I bending( /~/ . bent ng ~ ~:~:~ .... ~ ...

~ ] ~ f b '~ ~ '~/pressure ~ : ,ressure I,~ ~p il pressure 1/""~] ~ i ~'~inereased ~A~_ , ! nereased [~" ~[d=reased

d°Wn:l I:ddwn: I: :i

FIG. 5. The movements of the hyoid bone, thyroid and cricoid cartilages, after contraction of (A) sternohyoid muscle (SH), (B) sternothyroid muscle (ST), and (C) thyrohyoid muscle for C. CTD = cricothyroid distance.

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THE STRAP MUSCLES 31

the vocal folds. Another possible mechanism affect- ing the pitch during sternohyoid and sternothyroid contraction might be the effect of laryngotracheal forward bending. During lowering of the larynx af- ter contraction of these muscles, the cricoid carti- lage moves toward the cervical vertebrae and the thyroid cartilage moves anterocaudally. This results in shortening of the cricothyroid distance causing an increase in the length and tension of the vocal folds.

We can explain the different results of pitch be- tween the sternohyoid and sternothyroid muscles on an anatomical basis. The sternohyoid muscle is the largest among the strap muscles and takes its origin from the posteromedial surface of the clavicle and sternum and is inserted into the inferior border of the body of the hyoid bone. The sternothyroid muscle runs from the upper posterior part of the clavicle and sternum to the oblique line of the thy- roid lamina. The oblique line is roughly equidistant from the isthmus of the thyroid laminae and cri- coarytenodi joint. When these muscles contract, the thyroid cartilage rotates downward around the cricothyroid joint and the anterior part of the cricoid cartilage comes closer to the thyroid and the arytenoid cartilages. In this study, the stenothyroid muscle showed less effective pitch raising than the sternohyoid muscle. We suggest that this difference might be due to the directions of muscle contrac- tion. The more anteriorly directed of the two mus- cles is the sternohyoid muscle. Thus, the contrac- tion of the sternothyroid muscle resulted in less de- gree of laryngotracheal pull and bending than the sternohyoid muscle.

On the other hand, the thyrohyoid muscle acted to lower the pitch. The thyrohyoid muscle runs from the oblique line on the thyroid cartilage to the hyoid bone and when contracted may move both the hyoid bone and the thyroid cartilage. The at- tachment of the thyrohyoid muscle at the oblique line enhances the ability to deflect the thyroid car- tilage inward and upward. In this study, the crico- thyroid distance was increased. This effect seems to the related to laryngotracheal upward pull and not laryngotracheal bending. The cricoid and thyroid cartilages moved upward together, but the thyroid cartilage moved more cranially than the cricoid car- tilage because the cricoid cartilage is relatively fixed to the adjacent connective tissue. Another possible mechanism of lowering the pitch and vocal intensity might be lowered subglottic pressure.

In conclusion, the contraction of the sternohyoid

muscles caused the laryngotracheal downward pull and high air volume in the subgiottic air space, and correspond to increasing the subglottic pressure. This downward pull resulted in shortening the cricothyroid distance; anterior downward bending caused shortening of the anterior cricothyroid dis- tance and resulted in lengthening the vocal folds and raising the frequency. The contraction of the sternothyroid muscle also resulted in raising F0, but less than the sternohyoid muscle because the laryn- gotracheal pull and bending was less prominant, which was most likely due to the direction of mus- cle pull. The contraction of the thyrohyoid muscle caused the larynx to move upward. The thyrohyoid muscle made the thyroid cartilage move more up- ward than the cricoid cartilage and caused length- ening of the anterior cricothyroid distance, resulting in lowering of the frequency by decreasing vocal fold tension. It also caused lower air volume in the subglottic air space, and corresponded to decreased subglottic pressure and pitch.

Acknowledgment: This research was supported by the NIDCD Grant No. ROlDC0085-01 and by Veterans Ad- ministration Merit Review Funds. This study was per- formed in accordance with the PHS Policy on Human Care and Use of Laboratory Animals, the NIH Guide for the Care and Use of Laboratory Animals, and the Animal Welfare Act (7 U.S.C. et sequ.); this animal use protocol was approved by the Institutional Animal Care and Use Committee (IACUC) of the University of California, Los Angeles.

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