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Journal of Voice

Vol. 3, No. 3, pp. 213-224


© 1989 Raven Press, Ltd., New York

Role of the Thyroarytenoid Muscle in Regulation of


Fundamental Frequency

Ingo R. Titze, Erich S. Luschei, and *Minoru Hirano


Department of Speech Pathology and Audiology, The University of Iowa, Iowa City, Iowa, U.S.A. and
*Department of Otolaryngology, Head and Neck Surgery, Kurume University, Kurume, Japan

Summary: Thyroarytenoid muscle activity is shown to combine with cricothy-


roid muscle activity to regulate fundamental frequency of phonation. The rel-
ative amount of activity in these muscles, as measured electromyographically,
is illustrated on a muscle activation plot (MAP) for four subjects vocalizing at
different pitches and loudnesses. Electrical stimulation of the thyroarytenoid
muscle in various regions of the MAP suggests that both positive and negative
changes in fundamental frequency (Fo) can occur with increased thy-
roarytenoid activity. At lower fundamental frequencies and lower vocal in-
tensities, Fo correlates positively with thyroarytenoid activity, but at higher
fundamental frequencies and low intensity (especially in falsetto voice) an
increase in thyroarytenoid activity tends to lower F o. A biomechanical body-
cover model of fundamental frequency control is used to explain this phenom-
enon. Key Words: Thyroarytenoid--Body-cover--EMG--Fundamental
frequency--Electrical stimulation--Pitch control.

The role of the thyroarytenoid (TA) muscle in proximately as the square root of the effective stiff-
fundamental frequency regulation is not fully under- ness (or equivalently, the effective longitudinal ten-
stood. As suggested by Hirano (1,2), the thy- sion).
roarytenoid muscle should be able to stiffen the The possibility of both positive and negative
body of the vocal fold while slackening the cover. changes of F o with increasing TA activity was re-
This nonuniform stiffening of adjacent vocal fold cently predicted quantitatively by Titze, et al. (3) on
tissues, which presumably occurs most markedly the basis of rotational equilibrium mechanics
when the vocal fold is allowed to shorten, creates around the cricothyroid (CT)joint. The mechanical
an uncertainty about the effective stiffness of the properties were based on measurements made on
tissue in vibration. If the vibrating cross-sectional three canine larynges in vivo and several samples of
area is primarily nonmuscular tissue (cover), then muscle tissue in vitro. The approach showed con-
the effective stiffness should be lowered by TA con- siderable promise for quantifying the body-cover
traction. On the other hand, if the vibrating cross- theory of Fo control, but more data are needed to
sectional area is primarily muscular tissue, then the raise the confidence level of the results. More im-
effective stiffness could be raised. The fundamental portantly, the canine larynx is not an ideal model of
frequency (Fo) would be expected to change ap- the human larynx when vocal fold tissue morphol-
ogy is in question. Owing to the virtual absence of
the vocal ligament in the canine (1), the cover seems
to be more loosely connected to the body in the dog
Address correspondence and reprint requests to Dr. Ingo R.
Titze, Dept. of Speech Pathology and Audiology, The University than in the human. This makes the distribution of
of Iowa, Iowa City, IA 52242, U.S.A. cover tissue and body tissue in the vibrating portion

213
214 I . R . TITZE E T A L .

of the vocal fold potentially different in the two spe- thyroarytenoid and cricothyroid muscles of each
cies. subject. The electrodes were made by passing two
Given this morphological difference, we felt it ap- 0.003-in diameter, Teflon-insulated, stainless steel
propriate to test the preliminary results obtained wires through a 1.5-in 25-gauge hypodermic needle.
with the canine model on some human subjects be- The distal 1-2 mm of the end of each wire was bared
fore a larger study with more animals was initiated. of insulation by scraping or heating and was then
A clear disadvantage in the use of human subjects is formed into a hook. The electrodes were sterilized
that no direct mechanical quantities, such as force, by autoclaving. The skin at the penetration site over
elongation, or vibrating cross section, can be mea- the lower portion of the laryngeal framework was
sured easily. The protocol outlined in this study is anesthetized by a small subcutaneous injection of
therefore designed to give only indirect confirma- lidocaine. The electrodes were inserted through the
tion of the amount of involvement of the body and skin and directed into the appropriate muscles. All
cover. It provides some qualitative assurance that insertions were performed by one of the authors
future refinement with the animal model is justified. (M.H.), who has extensive experience with this
Our assumption is that low-intensity and high F o procedure. The location of the electrodes was eval-
phonation involves less of the body in vibration uated by observing the electromyographic activity
than high-intensity and low F 0 phonation. This as- (EMG) recorded from the electrode pair during var-
sumption is based simply on differences in vibra- ious maneuvers. High levels of EMG during closure
tional amplitude. Loud and low phonations have of the glottis (swallowing, glottal attack, valsalva)
greater amplitudes of vibration than soft and high were considered to be from the thyroarytenoid.
phonations. By examining the effective depth of vi- EMG activity that increased when the pitch of vo-
bration with the use of videostroboscopy, the calization was raised was considered to be from the
amount of involvement of the body in vibration was cricothyroid. If EMG increased during depression
assessed (qualitatively). The basic hypotheses of the chin against a manual force, it was assumed
were: that the electrodes were picking up strap muscle
activity. Such electrodes were removed and new
(a) F0 changes with increased TA tension should electrodes inserted.
be more positive when amplitude of vibration is In the first part of the procedure, EMG activity
high than when amplitude of vibration is low. was recorded on an instrumentation tape recorder
(b) F 0 changes with increased TA tension should (DC-2.5 kHz bandpass) while the subject main-
be more positive when CT activity is low than when tained phonation at various low, middle, or high
CT activity is high. pitches. At each pitch, the subject produced pho-
nation in four ways: soft, medium, and loud levels
The second hypothesis grew directly out of the of intensity, and in some cases a soft breathy voice.
consideration that, at low CT activity, the TA mus- Each phonation was approximately 4-6 s long, ex-
cle is more able to increase the net tension of the cept for " b r e a t h y , " which was typically much
vibrating portion of the vocal fold because the ten- shorter. Three or four tokens were recorded for
sion in the cover is rather low. At high CT activity, each condition. Constancy of pitch during the four
on the other hand, when the tension in the cover is conditions was established by having the subject
quite large, it is difficult for the body to bring about listen to a pitchpipe between tokens. The exact low,
a substantial increase in the net tension of the vi- middle, and high pitch used with each subject dif-
brating system. fered somewhat; the pitches chosen were the ones
that the subject found relatively easy to maintain,
METHODS AND PROCEDURE but typically covered one octave or more.
The EMG was additionally recorded during swal-
Four adult males, ranging in age from 28 to 47 lowing, glottal attack, voluntary glottal adduction,
years, served as subjects for the study. None had singing scales over the entire pitch range, and the
any known vocal pathology at the time of the ex- production of swell-tones.
periment. Two subjects had had extensive training After EMG activity had been recorded during all
and experience as singers, whereas the other two of the above conditions, the electrodes to the thy-
had had no voice training. roarytenoid were connected to an isolated, con-
Bipolar fine wire electrodes were placed in the stant-current electrical stimulator. One millisecond

Journal of Voice, Vol. 3, No. 3, 1989


THYROARYTENOID M U S C L E A N D F U N D A M E N T A L F R E Q U E N C Y 215

pulses were delivered to the thyroarytenoid at a rate tivation plot (MAP) for each of the four subjects in
of 2/s during phonation at each pitch and loudness. Figs. 1--4. Figures 1 and 2 are for the two untrained
The current level was set for each subject by finding vocalists and Figs. 3 and 4 are for the two trained
a level that subjectively produced a twitch in the vocalists. For each MAP, activity in the cricothy-
throat, but that did not cause pain; currents ranged roid muscle (act) is plotted against activity in the
from 1-7 mA among the subjects. Once the stimulus thyroarytenoid muscle (ata). Both muscle activities
current was set for any one subject, however, it was are normalized to maximum activity, which is as-
held at that level for all phonations. Approximately signed the value 1.0. The subjects' fundamental fre-
100 stimuli were recorded during each pitch- quencies (in hertz) are shown for pairs of data
loudness combination, except for " b r e a t h y , " in points connected by lines. Arrows within each pair
which about 50 stimuli were recorded. An electro- represent the direction in which loudness was in-
glottographic signal (EGG), low-pass filtered creased at a given fundamental frequency. For all
slightly above/70, was recorded during the stimula- subjects (except SA in Fig. 3), two pairs of data
tion procedure for later F0 extraction. points were obtained by repeating the experiment
The relationship between EMG activity and all of with new EMG insertions. The two experimental
the pitch-loudness combinations, as well as other sessions were conducted 9 months apart.
maneuvers, was studied by playing out the rectified A first observation is that none of the subjects
(but unfiltered) EMG records on a direct-writing os- show pronounced activity in the lower right quad-
cillograph, which had a frequency response of DC rant of the tensor MAP. This is apparently the glot-
to 2 kHz. The average amplitude of the EMG was tal stop region, where act is small and ata is large,
measured during each pitch-loudness combination. resulting in hyperadducted vocal folds that are un-
In the case of the thyroarytenoid, the measure- likely to produce phonation.
ments were normalized to the EMG amplitude as- Subjects JJ and EL (Figs. 1 and 2, respectively)
sociated with swallowing. Cricothyroid was nor- sometimes found it difficult to maintain a given
malized to the level for the highest tone in the pitch when loudness was increased. Subject JJ had
scales. For one subject (IT), however, both CT and a range of about one and a half octaves (131-392
TA activities were renormalized to a loud G 4 tone
because activities for this experimental tone were
greater than for swallow or for the highest tone in 1.0
C=O
the preliminary scales. 262 Hz
Changes in the fundamental frequency of phona-
tion, AFo, produced by the electrical stimulation of 0.8
the thyroarytenoid, were studied by triggering an 8Q~O 392 ----e
oscilloscope from each cycle of the EGG and using /.
the horizontal gate pulse from the oscilloscope as an 0.6
input to an instantaneous frequency meter. The full
range of the meter was set to 200 Hz for low e"
pitches, and to 600 Hz for all higher pitches. The
0.4
output of the frequency meter was averaged by a
laboratory computer, synchronized by stimulus
time marks that had been recorded on the tape re-
corder. Fifty stimuli were generally included in
o. f y
each average. There were two independent aver-
ages from each condition, except for "breathy."
These two averages were almost always very simi- 0.0 . . . . . '~ . . . . . . . . .
0.0 0.2 0.4 0.6 0.8 1.0
lar to one another.
ata
FIG. 1. Muscle activation plot (MAP) for subject JJ, an un-
RESULTS trained vocalist. Open circles are for first experimental session,
and filled circles are for second experimental session. Funda-
EMG mental frequencies in hertz are indicated for each pair of soft-
loud phonations. Arrows point in the direction from soft to loud.
The EMG data for the vocal fold tensor muscles Cricothyroid muscle activity act and thyroarytenoid muscle ac-
CT and TA are shown graphically on a muscle ac- tivity ata are normalized to the maximum value observed.

Journal of Voice, Vol. 3, No. 3, 1989


216 I . R . TITZE ET AL.

1.0 U Thyroarytenoid stimulation


440 Hz
As described in Methods and Procedure, the TA
44O
muscle was stimulated in all subjects. Only one sub-
0.8 ject (EL) showed consistently large changes in F o
with moderate to low currents (<5 mA). It is con-
ceivable that the insertions for this subject were
0.6
~ 20
near a nerve ending and that, as a result, some ef-
fective nerve stimulation was achieved. The F o
changes are shown graphically in Fig. 5 for several
0.4 pitch and loudness conditions. An additional nu-
merical summary of the F 0 changes is given in Table
1. In approximately one-half of the conditions, two
independent experiments (involving different elec-
0.2
trode insertions approximately 9 months apart) are
represented as data pairs, both in Fig. 5 and Table
1. It was felt that this verification was needed to
0.0 I , : ', : : : I : : I : : : I : : :
0.0 0.2 0.4 0.6 0.8 1.0 raise the confidence level in the results.
ata
TA stimulation produced a consistently positive
FIG. 2. Muscle activation plot (MAP) for subject EL, an un-
AF0 in the low to medium low pitch range (G2 -- 98
trained vocalist. Open circles are for first experimental session, Hz to E 3 = 164 Hz). This is in the speech quadrant
and filled circles are for second experimental session. Funda- of the MAP, where activity levels of both TA and
mental frequencies in hertz are indicated for each pair of soft-
loud phonations. Arrows point in the direction from soft to loud.
CT are below 0.5. Negative AF0 was observed at
Cricothyroid muscle activity act and thyroarytenoid muscle ac- very high pitches ( A n = 440 Hz), where CT con-
tivity ata are normalized to the maximum value observed. traction was near 1.0. These were falsetto (or near
falsetto) phonations, where TA muscle activity was
less than CT muscle activity. In the medium pitch
Hz), whereas subject EL phonated over more than range ( A 3 = 220 Hz to E 4 = 330 Hz), the funda-
two octaves (98-440 Hz). Neither of them showed
consistent EMG trends with increasing loudness.
Both CT and TA activity seemed to increase or de- 1.0
crease in unsystematic ways from soft to loud pho-
nation at given pitch levels. The trained vocalists,
on the other hand, showed more consistent in- 0.8
creases in TA activity with increasing loudness.
More will be said about loudness regulation in later
discussions. 0.6
All subjects were able to cover the male speech
range of F0 (from below 100 Hz to about 250 Hz) ~d
with act and ata both less than 0.5 (in the lower left 0.4
quadrant of the MAP). This quadrant of the MAP
will be called the speech quadrant. As Fo is raised in
chest register, the tendency is to move diagonally
0.2
from the lower left quadrant to the upper right quad-
rant (both act and ata greater than 0.5) for all sub-
jects. As the phonation becomes more falsetto-like,
0,0 I . . , ! •. . • . .• i

however, the tendency is toward the upper left 0.0 0.2 0.4 0.8 0.8 1.0
quadrant, where ata < 0.5 a n d act > 0.5. It would
appear that the upper two quadrants are where ma- FIG. 3. Muscle activation plot (MAP) for subject SA, a trained
jor register transitions would take place in singing, vocalist. Fundamental frequencies in hertz are indicated for each
with the falsetto-head transitions occurring in the pair of soft-loud phonations. Arrows point in the direction from
soft to loud. Cricothyroid muscle activity act and thyroarytenoid
upper left quadrant and the head-chest transition muscle activity ata are normalized to the maximum value ob-
occurring in the upper right quadrant. served.

Journal of Voice, Vol. 3, No. 3, 1989


THYROARYTENOID MUSCLE AND FUNDAMENTAL FREQUENCY 217

1.o token with repeated stimulation at 2 Hz. Either the


placement of the electrodes, the amount of current
delivered, or the time-varying properties of the con-
0.8 tracting muscle were less than ideal for obtaining
large twitches. There were also measurement arti-
e..4~nO 440 830
facts. For the two singers, the presence of vibrato
0.6 compromised our ability to line up and average F o
variations that could be attributed solely to the mus-
-a -~--~'ll" 0 -0330
0a cle twitch. In addition, for subject IT an initial pos-
9200.,.. o 862
0.4
itive AF0 was sometimes followed by a negative AFo
~l t85 in a period of about 100 ms (Fig. 6). This biphasic
~g165 frequency change, which occurred mainly at low
frequencies, is observable also in the data of Larson
0.2
and Kempster (4). It may suggest that tension in the
t8131 TA muscle first increases isometrically, but then
decreases when the vocal folds shorten. There is no
0.0 : : : : : : : : : : : : :
secondary evidence for this, however, and other
0.0 0.2 0.4 0.6 0.8 1.0
explanations could possibly be given. In any case, it
FIG. 4. Muscle activation plot (MAP) for subject IT, a trained was difficult to assign a net positive or negative AFo
vocalist. Empty circles are for first experimental session, and in these responses.
filled circles are for second experimental session. Fundamental Table 2 shows a summary of results for subject
frequencies in hertz are indicated for each pair of soft-loud pho-
nations. Arrows point in the direction from soft to loud. Crico- IT, one of the two subjects with voice training. In
thyroid muscle activity act and thyroarytenoid muscle activity ata the middle of the fundamental frequency range,
are normalized to the maximum value observed. subject IT demonstrated primarily small negative
changes in F0. According to our two hypotheses,
this would mean that either his TA muscle was not
mental frequency change was sometimes positive involved much in vibration (because of small ampli-
and sometimes negative. Wherever a discrepancy tudes), or that the vocal fold cover remained quite
existed, however, the softer phonations produced a stiff throughout all the phonations. Given that the
less positive (or negative) AFo. In the A 3 and E 4 productions were perceived to be quite intense
tones in Fig. 5, soft phonation produced a AFo of (both from a muscular effort and an auditory point
- 1 6 Hz and - 1 7 Hz, respectively. These are ap- of view), the second explanation involving a gener-
parently cases for which the cover was primarily in ally stiff cover seems more plausible. Thus two con-
vibration. Stimulation of the TA muscle probably trasting tissue morphologies may be manifested in
shortened the vocal folds, thereby slackening the subjects EL and IT, giving rise to an almost in-
cover and reducing tension. For loud phonation on verted AF0 pattern over the intensity and frequency
the same frequencies, a strong positive AF0 was ranges. If we assume that EL has a relatively lax
seen, which suggests that part of the body was in cover, small amounts of thyroarytenoid stimulation
vibration. These results (from this subject) begin to would raise the overall stiffness of the vocal folds
support our two basic hypotheses, that changes in isometrically and produce primarily positive F 0
F o with changes in TA activity should be more pos- changes. In contrast, if we assume that subject IT
itive when CT activity is low or when vibrational has a relatively stiff cover, small amounts of thy-
amplitude is large. It will be shown in the next sec- roarytenoid stimulation will not add much stiffness
tion that vibrational amplitude did indeed increase to the vibrating tissue, but may cause a small length
with loudness in this subject. reduction. This in turn may reduce the tension in
Stimulation data from the other three subjects did the cover and lower the fundamental frequency.
not show such clear trends. First of all, the F 0 The explanation would also a c c o u n t f o r the
changes were generally smaller. Second, they were monophasic AFo for subject E L and the biphasic
more variable from token to token, and even within AFo for subject IT.
tokens. Sometimes a negative AF0 obtained at the The remaining two subjects had less complete
beginning of a sustained vowel token would disap- data sets for stimulation. Subject SA, whose thy-
pear (or even change sign) toward the end of the roarytenoid muscle was not stimulated in the sec-

Journal of Voice, Vol. 3, No. 3, 1989


218 I . R . TITZE E T A L .

Breathy Soft Medium Loud

A4 (440 Hz)

E4 (330 Hz)

Cr.,,
<1 A, (sZ0 Hz)

E, (164 Hz)

G, (98 Hz) _/-,.

Time t 200 ms '


FIG. 5. Change in fundamental frequency (AFo) with thyroarytenoid muscle stimulation for different pitches and loudnesses. The subject
is EL. Pairs of AF0 patterns indicate results for two experimental sessions, session one on top and session two on bottom.

ond experimental session (due to three unsuccessful ineffectively placed, or perhaps shorted out after
hooked-wire insertions), exhibited no changes in Fo EMG measurements. Nevertheless, the fragmen-
at high notes (F0 = 349 Hz) in the first experiment. tary stimulation data from subjects JJ and SA seem
In the middle of the frequency range (220 Hz), a + 6 to follow some of the trends observed in the other
Hz change was recorded at loud phonations, with subjects. JJ is similar to EL, with generally positive
no significant changes at soft phonation. At low AF0 over the low to middle frequency range. The
notes (117 Hz), small negative changes were en- trend for SA may be similar to that of IT because
countered over various intensities. These did not small negative frequency changes occur in the low
exceed 3 Hz in magnitude. Subject JJ exhibited no to middle Fo range, but the data are too sparse to
AFo at 262 Hz, 3-4 Hz increases at 196 Hz, and make a firm comparison.
10--27 Hz increases at 131 Hz, all in the first exper- It is interesting to compare our results on TA
imental session. In the second session, TA stimula- stimulation with those of Larson and Kempster and
tion produced no AF0 for subject JJ at any intensity their co-workers (4,5). Negative AF0 was observed
or frequency. We assumed that the electrodes were only once in each of their two studies, presumably

Journal of Voice, Vol. 3, No. 3, 1989


THYROAR YTENOID MUSCLE AND F U N D A M E N T A L F R E Q U E N C Y 219

TABLE 1. S u m m a r y o f A F o (in h e r t z ) f o r subject EL"

Fundamental
frequency Hertz Breathy Soft Medium Loud

A4 440 - 15 - 18
-20 - 10
E4 330 -- --
-17 +6
A3 220 + 17 +21 + 18
- 16 b - - +22

E3 164 + 16.5 + 17 +22.5 + 17


-- +24 -- +24
G2 98 +7.5 +9 + 16.5
-- + 14 + 13.5

" Upper and lower numbers refer to first and second experimental sessions, respec-
tively.
b V e r y soft.

because fundamental frequencies were kept in the source (B & K 4914) was used to illuminate the
speech range (lower left quadrant of the MAP). If vocal folds, and the image was recorded with a
we were to count "frequency of occurrence" of Storz Mini 9000 Solid State CCD video camera and
negative AF0 in the lower left quadrant across our a Panasonic NV-8950 VHS videocassette recorder.
four subjects, it would fall below 20%. It is likely, Subsequently, the maximum glottal width was mea-
therefore, that our results are not at odds with those sured on a TV monitor screen with calipers. Mea-
of Larson and Kempster, but simply reflect a wider surements were repeated and averaged over five
range of TA and CT activity in our study. Never- cycles. Normalization of the maximum glottal width
theless, the occasional occurrence of negative AF 0 to the loudest and lowest phonation was possible
in this speech range still needs clarification on phys- because this condition consistently produced the
iologic and biomechanical grounds. greatest values. We assume that the amplitude of
vibration is proportional to the maximum glottal
Vibrational amplitude and loudness width.
Three of the four subjects repeated some of the Figure 7 shows the results for the three subjects
phonations at previously described pitches and at three pitch levels; low, medium, and high. Rela-
ioudnesses while a rigid fiberscope (Wolf 4450-47) tive amplitude (normalized to the low-loud condi-
was inserted into the mouth and positioned near the tion) is plotted against three loudnesses; soft, me-
posterior pharyngeal wall. A stroboscopic light dium, and loud. Note that there is a uniform
increase in relative amplitude with increased loud-
ness. For all subjects, relative amplitude was great-
est for low pitch, less for medium pitch, and least
for high pitch. On the average, the relative ampli-
tude doubled (from 0.4 at soft phonation to 0.8 at
loud phonation) when data for all pitch levels and all
subjects were collapsed. Specifically for subject EL
(circles), relative amplitude increased from an av-
erage of 0.45 to an average of 0.90 when the data
were collapsed over all pitch conditions. Thus we
can assume a 2:1 increase in amplitude from soft to
loud in subsequent discussions.

A MODEL OF FUNDAMENTAL
50 100 1,~0 200
FREQUENCY REGULATION
Time in ms In a previous study (3), we derived an equation
F I G . 6. B i p h a s i c A F o p a t t e r n o b s e r v e d in s u b j e c t IT. relating vocal fold strain e to thyroarytenoid muscle

Journal of Voice, Vol. 3, No. 3, 1989


220 I . R . TITZE E T AL.

TABLE 2. Summary of M~ofor subject 17~


Fundamental
frequency Hertz Breathy Soft Loud
A4 440
G4 392 + 13 positive phase 1 First --
- 2 negative phase J~ experimental
session
+ 10 positive phase ] Second
- 8 negative phase f experimental
session
E4 330 -4 --
Ca 262 - 4.5 - 2
A3 220 - 3.5 -3
E3 165 - 1 - 2.5
D3 147 +8 -- --
C3 131 -3 --
G2 98 + 3.5 positive phase + 2 positive phase
- 4 . 0 negative phase - 5 negative phase
a Except where indicated, results are for the first experimental session.

activity ata and cricothyroid muscle activity act in g e o m e t r y , and m a x i m u m T A force p r o d u c e d . It


the canine larynx. The equation was is a m e a s u r e o f how sensitive vocal fold elongation
is to muscle contraction. F o r the canine larynx, G
= G(Ract - ata ) (1) and R were found to have dimensionless values of
where R is a torque ratio relating the m a x i m u m 0.10 and 3.5, respectively. F o r the h u m a n larynx,
torque that can be produced by the CT muscle to the torque ratio of 3.5 seems to be appropriate, but
the m a x i m u m opposite torque that can be produced a higher gain (G = 0.17) is needed to achieve fun-
by the T A muscle. (The torque axis passes through d a m e n t a l f r e q u e n c i e s ranging f r o m a b o u t 50 to
the CT joints.) R can be thought of as a mechanical 500 Hz.
advantage that CT has o v e r TA. G in Eq. 1 is a gain The fundamental frequency was derived to be
factor that depends on rotational stiffness, laryngeal I/2

1.0 m
Fo = Fop
( 1 + A O'p ata
t (2)

where Fop is the passive f u n d a m e n t a l frequency


(when there is no thyroarytenoid contraction), Aa/A
O.S is the ratio of the cross section of the T A muscle in
vibration to the total cross-sectional area in vibra-
/ .j'j,. "-" ,, tion, O-am is the m a x i m u m active stress (force per
0.6, unit area) in the T A muscle, and O-p is the mean
passive stress of all the c o m b i n e d tissues in vibra-
E!
/ tion.
/ / .
0.4. Four auxiliary equations

Ili
L = L0(1 + ~ - 0.623) (3)

0.2.
O-p = 104 e 9-2~ dyn/cm 2 (4)

O'am = 106(1 + 0 . 6 e ) d y n / c m 2 (5)

o.o I I I Fop = (1/2L)(o-p/p)'/2 (6)


Soft Medium Loud
were also introduced in the previous paper. In Eq.
FIG. 7. Relative amplitude of vibration versus loudness condi- 3, L is the m e m b r a n o u s vocal fold length at any
tion for three subjects at low pitch (short dashed lines), medium
pitch (long dashed lines), and high pitch (solid lines). Circles are given strain e, with L0 being the reference length
for subject EL, triangles for SA, and squares for JJ. (1.6 c m for m a l e s on a v e r a g e and 1.0 c m for

Journal of Voice, Vol. 3, No. 3, 1989


THYROARYTENOID MUSCLE AND FUNDAMENTAL FREQUENCY 221

females). The factor -0.623 is necessary to trans- motor system is dealing with a peripheral mecha-
form typical strains used in in vivo dog experiments nism that offers multiple solutions to accomplish
to typical strains found in human vocal fold length the same task. These redundancies may be re-
adjustments (6). In Eq. 4, the passive tissue stress is moved, however, when more stringent require-
modeled with an exponential stress-strain curve ments are put on the vocalization, such as specific
(6,7), while in Eq. 5, the maximum active stress loudnesses, qualities, or dynamic Fo changes. For
follows the data on canines reported by Alipour- example, a 300 Hz tone may have distinctly differ-
Haghighi et al. (8). Finally, Eq. 6 is the familiar ent qualities in the three quadrants. It is likely to be
formula for the fundamental frequency of a vibrat- a falsetto sound in the upper left quadrant, a chest
ing string, p being the tissue density (1.03 g/cm3). sound in the upper right quadrant, and a pressed
Equations 1 through 6 can be combined to yield sound in the lower left quadrant.
one equation in four unknowns, act, ata, Fo, and The second point to make is that changes in Fo
Aa/A. In the process, the variables L, o-0, O'am, 6, and with increased TA activity are all positive in the
Fop are eliminated by substitution. In order to relate lower left quadrant. A positive increment in ata (to-
the theoretical results to experimental results dis- ward the right) will approach a higher F 0 curve,
cussed earlier in Figs. 1-4, it is useful to obtain a both for the solid lines (soft phonation) and the
theoretical MAP by solving for act as a function of dashed lines (loud phonation). This is a direct result
ata, with Fo and AJA being parameters. This re- of the downward bending of the curves in the lower
quires a numerical solution of Eqs. 1 through 6 be- left quadrant. Similar statements can be made about
cause some of the equations are transcendental in 6. the lower right quadrant, but phonation generally
Such a numerical solution is shown graphically in does not occur in this " s t o p " region. Near the top
Fig. 8. Normalized cricothyroid activity act is plot- of the upper quadrants, AFo can be negative with
ted against normalized thyroarytenoid activity ata, increased ata. Displacement to the right from a
with families of curves representing constant F0 given Fo curve will approach a lower Fo if the
contours. Fo varies in 50 Hz increments from a low curves have a positive slope. Thus, F 0 and ata are
of 100 Hz (lower left corner) to a high of 450 Hz inversely related at the higher frequencies, espe-
(upper left corner). Solid lines are for AJA -- 0.3 cially for A j A = 0.3 (solid lines corresponding to
and dashed lines are for AJA = 0.6. These ratios soft phonation).
are estimates to represent the soft and loud condi- This theoretical result agrees with experimental
tions, respectively, in the experimental data. In findings on subject EL. Note that the two 440 Hz
other words, less than one-third of the vibrating phonations in Fig. 2 occurred near the top of the
cross section is assumed to be TA muscle in soft MAP. Recall also that AFo was always negative for
phonation, whereas nearly two-thirds of the vibrat- this frequency with TA stimulation (Fig. 5 and Ta-
ing cross section is assumed to be muscle in loud ble 1). Although in Fig. 8 the 440 Hz curve is
phonation. This doubling of Aa/A agrees with the slightly off the graph above the upper right quad-
doubling of vibrational amplitude noted earlier. rant, it is evident that negative AFo would be pre-
Several observations are in order with regard to dicted for both sets of data, especially if Aa/A is
Fig. 8. First, the lowest Fos are attainable with low closer to the 0.3 value.
act and low ata (lower left quadrant of the MAP, The 350 Hz curve is even more interesting. Here
where speech is produced), highest F0s are attain- both positive and negative changes in F o are pre-
able with high act and low ata (upper left quadrant, dicted with increasing ate. Upward sloping lines in
where falsetto is produced), and intermediate Fos the upper left quadrant give rise to negative AF0
are found in all quadrants. Since the constant Fo with increasing ata for soft phonation, whereas the
lines are continuous, an infinite number of combi- downward sloping lines for loud phonation give rise
nations of CT and TA activity are possible for every to positive AF0. Experimental results from subject
F0. For example, 300 Hz can be obtained in the EL confirm this sign reversal. Note that AFo in,Fig.
Upper left quadrant with ata = 0 and act = 0.76. 5 (330 Hz) is negative for soft phonation and posi-
With only a gradual increase in act (solid line for tive for loud phonation. Muscle activity level was in
Aa/A = 0.3), ata can vary all the way into the upper the upper right quadrant (Fig. 2) for this frequency.
right quadrant. With a combined reduction in both In this same quadrant, Fig. 8 predicts opposite
act and ata , the 300 Hz curve extends all the way slopes for the soft and loud conditions at 350 Hz.
into the lower left quadrant. Thus we see that the Below 250 Hz, AF0 is predicted to be positive for

Journal of Voice, Vol. 3, No. 3, 1989


222 I . R . TITZE E T AL.

1.0

,%

t
I
0.8 I
% I
I
I
/
I /
• I~0 r,.
I #
,v ~ ... ~ . _ %
i ~i II /**
0.6
200 , ; \ I II i/0 I~, S-S*- -
/ t~ ,,," /
.' ,7 ., /
o:I ,, // ,so," ~ ' . . "
%%1 X ! / ) , ,'/ ,, /..
t60 ras i ~n / / / I/ ,, /,,,,
0.4. --
\
I
, |
/
, I, ,,/ , , , ' / , , " . . . /
I\
,l\~
i
,
Ik / I/ ,,'/,,"/,,," ,v"
i t' r ,
# //
l,-
,,/ / ~ . soo / /
,"/,'/," / ,,r/
i I I / /i
l l I ~ / 11./
I ! .1 I / f/ 111
0.2
,:. , / ;/ ,1 ,,' /,/,, , , // /. ,
/ / ,,
l '/,"I . . /"/," .//,',
,

t,11 11,' / I" t l,'/,"/,


/ [ #" • /•
/! /l,'i " .'/,',~"
0 0.2 0,4 0.8 0.8 1.0

ata
FIG. 8. Theoretical muscle activation plot (MAP). Solid lines of constant F o are for Aa/A = 0.3 and dashed lines for A./A = 0.6.

all loudness conditions. This is again in agreement increased loudness (horizontal or slightly rising or
with Fig. 5, with the exception of one very soft falling lines in Figs. 3 and 4), excepting a few data
phonation in experimental session two that showed pairs in the lower left quadrant for subject IT. It
a negative AF0 at 220 Hz. However, a slightly appears that increased TA activity is used by sing-
louder phonation in experimental session one ers in conjunction with the major mechanism for
showed the predicted result. This suggests that the increasing loudness, increased subgtottal pressure.
model is quite accurate in explaining the general Much less systematic approaches were observed
direction of F o change in various quadrants. for the two nonsingers (Figs. 1 and 2). Furthermore,
A final point of interest is the mechanism by the singers kept the CT activity more constant,
which loudness is increased at constant fundamen- even though some changes in both directions were
tal frequency. Recall that the trained subjects SA observed.
and IT systematically increased TA activity with In previous EMG studies of singers performing a

Journal o f Voice, Vol. 3, No. 3, 1989


THYROARYTENOID MUSCLE AND FUNDAMENTAL FREQUENCY 223

crescendo at constant pitch (9,10), the CT activity which the basic model was derived. It remains to be
usually decreased while the TA activity increased. seen if adjustments in biomechanical and geometric
This indicated that pulmonary pressure was one of parameters of the model can be made to match the
the major mechanisms for increasing loudness. response of any human larynx, and if better re-
Given that F0 increases at a rate of 2-6 Hz/cm H20 sponses to stimulation can be obtained.
with increased subglottal pressure (11), some F0 Notwithstanding some of these limitations, the
compensation can be achieved by reduced CT ac- present study has shed considerable light on the
tivity. Figure 8 predicts that crescendos at constant mechanism of F o regulation. An explanation has
F0 should be trajectories between the solid lines and been offered for why increased thyroarytenoid mus-
the dashed lines if pulmonary pressure is increased cle activity can both raise and lower Fo. When the
and the amplitude of vibration grows. Should TA cover is lax and the amplitude of vibration is suffi-
activity stay constant in the process, the trajecto- ciently large to include a portion of the muscle in
ries would be vertical (downward). This implies an vibration, increased thyroarytenoid activity will
automatic reduction in CT. If TA activity is in- raise F 0. This is because the increase in tension in
creased together with pulmonary pressure, the tra- the muscle outweighs the decrease in the tension in
jectories are sloping or straight lines from left to the cover that may result from a small decrease in
right, as in the data of subjects SA and IT. The vocal fold length. This effect increases with increas-
slopes of the trajectories should be positive at high ing vibrational amplitude, i.e., with increased loud-
F0 and zero or slightly negative at intermediate F0s. ness, because more of the muscle is involved in
At low fundamental frequencies, the situation is vibration. Presumably, this situation is most often
more complicated because of the highly curved na- encountered in speech. It accounts for the generally
ture of the constant F o lines in Fig. 8. In the lower positive correlations observed between F0 and TA
left quadrant, it may be necessary for TA to de- in a speech environment (12,13). If the amplitude of
crease in order to follow a trajectory from the solid vibration is very small, such that none of the muscle
to the dashed line. is in motion, F o can only drop with increased TA
Given these many possibilities, it is not surprising activity. This is a plausible condition for the canine
that the subjects showed great variabilities in their larynx, in which the cover is 2-3 mm thick, but does
approaches to intensity control, especially the un- not appear to be a plausible condition in the human
trained vocalists. A next step in the experimental larynx. The presence of the vocal ligament and the
protocol would be to include subglottai pressure as thinner cover (about 1 mm) would seem to prevent
a controlled variable. This would increase the com- this complete independence of the body and cover
plexity of the experiment, but would add consider- in humans.
able insight into both frequency and intensity con- When the cover is very tense (large cricothyroid
trol. activity with elongated vocal folds), the active ten-
sion in the TA muscle cannot match the tension in
DISCUSSION AND CONCLUSIONS the cover and the vocal ligament. Greater contrac-
tion of the muscle will lower F o because the small
The results of this study are both satisfying and gain in muscle tension is outweighed by reduced
slightly disappointing. It is unfortunate that only tension in the cover that results from a small de-
one out of four subjects showed large and consis- crease in length. The length-tension curve for the
tent changes in fundamental frequency with stimu- cover is very steep at large elongations, making the
lation of the thyroarytenoid muscle. This leaves the loss of tension very dramatic with only minor re-
general applicability of our biomechanical model of ductions in length. At intermediate levels of CT and
fundamental frequency control in some doubt at TA contraction, our results show that an increase in
this time. On the other hand, the model has not TA can both raise and lower F 0. This depends crit-
been invalidated by those data sets that showed the ically on the amount of muscle in vibration~ For
strongest and most consistent trends. Both of the louder phonations, where the vibrational amplitude
specific hypotheses stated in the introduction were is larger, there is more likely to be an F 0 rise.
supported by theory and measurement. We might A next step in the development of this model is to
safely say that we have modeled the Fo control include the dependency of Fo on pulmonary pres-
mechanism for a single subject. Perhaps this sub- sure. The important link is the amplitude of vibra-
ject's larynx is closest to the canine larynx from tion, which needs to be quantified in detail. Recent

Journal of Voice, Vol. 3, No. 3, 1989


224 I . R . TITZE ET AL.

experimentation on excised larynges (7,11) has 4. Larson CR, Kempster GB. Voice fundamental frequency
changes following discharge of laryngeal motor units. In:
shown that changes in Fo with subglottal pressure Titze IR, Scherer RC, eds. Vocal fold physiology: biome.
can be accounted for by dynamic (or amplitude- chanics, acoustics, and phonatory control. Denver: The
dependent) stiffness in the vocal fold tissue. Denver Center for the Performing Arts 1983:91-104.
5. Kempster GB, Larson CR, Kistler MK. Effects of electrical
stimulation of cricothyroid and thyroarytenoid muscles on
Acknowledgment: This research was supported by the voice fundamental frequency. J Voice 1988;2:221-9.
National Institutes of Health, Grant No. NS 16320-08. 6. Titze IR. Physiologic and acoustic differences between male
The authors appreciate the assistance of David Druker, and female voices. J Acoust Soc A m 1989;85 (in press).
Steve Austin, and Linnie Southard in preparation of the 7. Titze IR, Durham P. Passive mechanisms influencingfunda-
manuscript and data reduction. We are also grateful for mental frequency control. In: Baer T, Sasaki C, Harris KS,
the many helpful suggestions and stimulating thoughts eds. Laryngeal function in phonation and respiration. Bos-
that were provided by Ronald Scherer, Ph.D., and David ton: Little, Brown, 1987:291-303.
Garrett, Ph.D. Finally, the medical assistance of Steven 8. Alipour-Haghighi F, Titze IR, Perlman AL. Tetanic contrac-
Gray, M.D. and his assistants from the Department of tion in vocal fold muscle. J Speech Hear Res (in press).
Otolaryngology-Head and Neck Surgery at the Univer- 9. Hirano M, Vennard W, Ohala J. Regulation of register,
sity of Iowa are greatly appreciated. pitch, and intensity of voice. Folia Phoniatr (Basel) 1970;
27:1-20.
10. Hirano M. Vocal mechanisms in singing: laryngological and
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Journal of Voice, Vol. 3, No. 3, 1989

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