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A reflex resonance model of vocal vibrato

Ingo R. Titze

National Center for Voice and Speech, and Department of Speech Pathology and Audiology, The University of Iowa, Iowa City, Iowa 52242 and, Wilbur James Gould Voice Center, Denver Center for the Performing Arts, Denver, Colorado 60204

Brad Story

National Center for Voice and Speech, The University of Iowa, Iowa City, Iowa 52242 and Speech and Hearing Sciences, University of Arizona, Tucson, Arizona 85721

Marshall Smith

National Center for Voice and Speech, The University of Iowa, Iowa City, Iowa 52242 and School of Medicine, University of Utah, Salt Lake City, Utah 84112

Russel Long

National Center for Voice and Speech, The University of Iowa, Iowa City, Iowa 52242 and Wilbur James Gould Voice Center, Denver Center for the Performing Arts, Denver, Colorado 60204

Received 6 November 2000; revised 30 October 2001; accepted 19 November 2001

A reflex mechanism with a long latency ( 40 ms) is implicated as a plausible cause of vocal vibrato. At least one pair of agonist–antagonist muscles that can change vocal-fold length is needed, such as the cricothyroid muscle paired with the thyroarytenoid muscle, or the cricothyroid muscle paired with the lateral cricoarytenoid muscle or a strap muscle. Such an agonist–antagonist muscle pair can produce negative feedback instability in vocal-fold length with this long reflex latency, producing oscillations on the order of 5–7 Hz. It is shown that singers appear to increase the gain in the reflex loop to cultivate the vibrato, which grows out of a spectrum of 0–15-Hz physiologic tremors in raw form. © 2002 Acoustical Society of America. DOI: 10.1121/1.1434945

PACS numbers: 43.75.Bc, 43.75.Rs, 43.70.Aj, 43.70.Bk RDA

I. INTRODUCTION

Vibrato is an ornament of music that is used by both vocalists and instrumentalists. As a frequency modulation of the fundamental frequency, vibrato enriches the average spectral content of a sustained tone because the harmonics can sweep through acoustic resonances of the instrument. If executed correctly, vibrato draws no attention to itself, but rather enhances the quality of the sound. Listeners generally judge tones with vibrato as being more lively, freer from tension, and more filling of the performance space. But, ex- cessive vibrato creates the perception of instability, lack of clarity of pitch, and a general ‘‘muddiness’’ of the melodic line. Skilled performers know the bounds of vibrato, decreas- ing its extent during rapid melodic movement and increasing its extent during long, sustained passages when melody and vibrato are less likely to be confused. The classic studies by Seashore and his co-workers summarized by Seashore, 1938 are still cited often as key authoritative measurements of the acoustic characteris- tics of vocal vibrato. Seashore wrote, ‘‘A good vibrato is a pulsation of pitch, usually accompanied with synchronous pulsations of loudness and timbre, of such extent and rate as to give a pleasing flexibility, tenderness, and richness to the tone’’ p. 33 . Seashore showed examples of the acoustic characteris- tics of vocal and violin vibrato. He demonstrated that vocal vibrato extent varied significantly from note to note, with the average peak-to-peak variation being one semitone or one quarter tone from the mean F o . Seashore also mea-

sured the vibrato frequency. He reported an average of 6.5

Hz, with less note-to-note variability in this frequency than

in the extent. Not much has changed in the acoustic description of

vocal vibrato over the last two-thirds of a century. However, vibrato frequencies of classically trained singers have re- cently been reported slightly lower than in the Seashore stud- ies. To compare two notable tenors of the first and second half of the century, Caruso’s average vibrato frequency was 6.5 Hz Dejonkere, 1995 , whereas Pavarotti’s frequency has been measured at 5.5 Hz Keidar, Titze, and Timberlake, 1984 . Informally, many vocal pedagogues have observed by listening to old and new recordings of identical pieces that vibrato frequency has lowered from the pre-World War

II era to the end of the 20th century. There are no compelling

explanations, but perhaps a preference toward a more ‘‘settled’’ sound less overt expressions of emotion is a part of the trend. In Prame’s 1994 study, the average frequency of ten classically trained recording artists singing Schubert’s Ave Maria was 6.0 Hz not the same as the Bach–Gounod Ave Maria studied by Seashore . Prame noted that all of the sing- ers tended to raise their vibrato frequencies at the end of each note. In particular, the last four to five vibrato cycles typi- cally rose from 6.0 to 7.0 Hz. In the more central portion of the phrase, however, the frequency was often below 6.0 Hz, typically about 5.5 to 5.8 Hz. Physiologically, vibrato has been described as a sympa- thetic if not synergistic oscillation phenomenon among la- ryngeal muscles. Hirano 1995 pointed out that the crico-

2272 J. Acoust. Soc. Am. 111 (5), Pt. 1, May 2002

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thryoid CT muscle is always activated in an oscillatory fashion in vibrato, whereas the thyroarytenoid TA muscle and the lateral cricoarytenoid LCA muscles are usually but not always involved. It is possible that the CT muscle may even interact with a strap muscle e.g., the sternothyroid or the sternohyoid, which are known to lower the larynx, and thereby perhaps shorten the vocal-folds . Hirano also re- ported that there can be oscillatory movement of many sur- rounding structures, such as the pharyngeal walls, the velum, the tongue, the epiglottis, and the jaw. A particularly inter- esting aspect of his study was the declining vibrato fre- quency with age, which he reported to shift from 5.4 Hz at age 20 to 4.7 Hz at age 65, on average, for a group of 21 singers. This decline of about 1 Hz over half a lifespan agreed with earlier findings by Damste ´ et al. 1982 and later findings by Sundberg et al. 1998 . Both groups of authors measured the vibrato frequencies of several professional singers who recorded the same pieces several times over a span of 30–40 years. Summarizing the preliminary findings on the physiology of vocal vibrato in our own laboratory, Titze et al. 1994 observed a 5–6-Hz reflex resonance mechanism for vocal vibrato that involved the CT and TA muscles. The study was conducted only on one singer, an amateur tenor. Damped oscillation was postulated to result from a negative feedback loop of moderate gain, the nature of which will be explored in greater detail here. When combined with the mechanics of rotation and translation of the thyroid and cricoid cartilage relative to each other, Titze 1996 showed that oscillatory behavior in vocal-fold length, tension, and fundamental fre- quency could be simulated with a mathematical version of this reflex oscillator. Hsiao et al. 1988 showed that motor unit activity in the CT muscle was correlated with F o changes in vibrato, both for integrated electromyographic EMG activity and single motor unit activity. Such correla- tions were also evident in laryngeal tremors studied by Finnegan et al. 1995 , but the phase relations between CT, TA, and voice F o remained somewhat of a mystery. A complete physiologic model of vocal vibrato may eventually explain the following empirical observations, mostly untested but somewhat agreed upon by singing teach- ers: 1 vibrato frequency is less controllable by the singer than vibrato extent; 2 many children and some adults sing vibrato-free; 3 many elderly or poorly conditioned vocalists have a slower and wider vibrato a wobble , which can be corrected by singing soft and high and by strengthening la- ryngeal muscles personal conversations with singing teach- ers ; 4 some young or muscularly hyperactive vocalists have an excessively fast vibrato a bleat that can be elimi- nated by singing in the midrange, using muscle relaxation exercises, and establishing a balanced vocal quality personal experience gained by the first author in training singers ; 5 training in general reduces the undesirable variability in vi- brato frequency; 6 violin, brass, or woodwind vibrato can be of similar rate as vocal vibrato, suggesting that the mass of the undulating structure e.g., the hand or respiratory bulk doesn’t dictate the rate as much as neurologic factors, as noted by Ramig and Shipp 1987 ; 7 some pathological vocal tremors are close to natural vibrato 5–6 Hz ; 8 vi-

J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002

brato rate often increases at the end of a note, as reported by Prame 1994 ; 9 vibrato occurs more naturally in the midrange of F o than at the extremes very low F o or very high F o ; and 10 vibrato rate can be entrained by an exter- nal stimulus Titze et al., 1994 . In this paper, we will ad- dress a few of these observations, but the investigation leaves many questions unanswered.

II. THE REFLEX RESONANCE MODEL

The proposed reflex resonance model for vibrato is sche- matized in Fig. 1. On the far right of the figure, the physi- ological processes are divided, from top down, into cortical activity, midbrain activity, and peripheral activity. The input to the model at the top is the pitch intended by the singer, with a vibrant quality but no deliberate attempt to create a vibrato. The output at the bottom is the fundamental fre- quency F o , which has a frequency modulation ranging be- tween 4–7 Hz, but the half-power bandwidth is more like 5–6 Hz. Cortically top third of the diagram , the motor program gets activated by auditory and kinesthetic memory of what a vibrant tone at a given pitch sounds and feels like, as well as the muscular effort and coordination it takes to produce it. In the process of organizing the muscle activations, central os- cillators are activated that superimpose a broad spectrum of physiologic tremor freqencies onto an otherwise constant level of activation Inbar and Eden, 1983; Elble and Koller, 1990 . The slightly tremorous motor activations to the CT and TA muscles are labeled A CT and A TA , respectively. The model is not limited to these two muscles. Other agonist– antagonist pairs e.g., a strap muscle working together with either the TA or CT, or the LCA working together with the CT could be engaged in this reflex resonance pairing, as long as they have an opposite effect on vocal-fold length and tension and thereby F o . In the midbrain center of the diagram , there is an inte- gration of sensory signals arriving from the laryngeal recep- tor organs muscle spindles, joint receptors, etc. and the cortical motor activations. The sensory-motor integration is symbolized by the summation signs and involves primarily corrective feedback in the form of time-delayed muscle strains 1 (t 1 ) and 2 (t 2 ), multiplied by their respec- tive gains g 1 and g 2 . The feedback-modulated activations are labeled a CT and a TA , respectively. The important model- ing parameters here are g 1 and g 2 , the feedback gains, and 1 and 2 , the feedback delays. These parameters will be given considerable attention in later discussions of experi- ments and modeling. At the periphery, the CT and TA muscles are now acti- vated with the modulated action potentials. This in turn modulates the vocal-fold length, which is quantified in terms of the vocal-fold strain , the elongation normalized to the resting length. If vocal-fold strain increases, the muscle spindles in the thyrovocalic portion of the TA muscle are activated Sanders et al., 1998 . With the appropriate gain g 2 and the reflex time delay 2 , this becomes the sensory modu- lation on the right side of Fig. 1 dashed lines . If the vocal- fold strain decreases, the muscle spindles in the TA are not activated, but joint receptors or spindles in the CT muscle

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FIG. 1. Block diagram of proposed reflex-resonance model of vocal vibrato. which is now stretched

FIG. 1. Block diagram of proposed reflex-resonance model of vocal vibrato.

which is now stretched are activated. In this case, the CT muscle strain 1 is not equal to the vocal-fold strain , but is a predictable function of it Titze, 1996 . With respective gain g 2 , this feedback becomes the sensory reflex modula- tion for the CT muscle on the left side of the figure, again shown in dashed lines. Concurrently, the vocal-fold strain determines the pas- sive tissue fiber stress in the vocal-fold, and the activation a TA determines the active stress in the muscular portion of the fold bottom three system blocks in Fig. 1 . Together, the two stresses govern the effective tension, and thereby the fundamental frequency F o . The basic hypothesis in this model is that the reflex gains and delays resonate, thereby tuning the broad spectrum of central tremor frequencies to a narrower band, which is known as vibrato illustrated in tem- poral and spectral form at the bottom of Fig. 1 . Thus, sing- ers with vibrato are expected to have a narrower bandwidth with correspondingly higher gains in the reflex loops than those who phonate without vibrato. The time course of events is hypothesized to be as in Fig. 2. Assume we begin with an increase in CT activation, represented by a small spike disturbance in Fig. 2 a at t 0. For simplicity, we illustrate all neural signals as single spikes, even though they are typically trains of spikes, within

2274 J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002

and across motor and sensory units. The single spike is con- sidered to represent the center of any train of action poten- tials. Below the spike shown in Fig. 2 a , a twitch-like con- traction occurs in the CT muscle Fig. 2 b , which reaches its peak about 33 ms after activation Perlman and Alipour- Haghighi, 1988 . The vocal-fold length strain increases in proportion to this contraction, with a small mechanical delay 10–20 ms , as shown in Fig. 2 c . This length increase trig- gers the TA muscle spindles, which are sensitive to both strain and strain rate ˙ Stein, 1982 . Spindle activation is shown in Fig. 2 d . The strain-rate dependence advances the phase, in part canceling out the mechanical delay in vocal- fold elongation, as observed by Stein. The major time delay now comes from the integration of the spindle sensory activation with the motor activation, which is labeled TA reflex motor activation in Fig. 2 e . The time delay is on the order of 40–50 ms, as we will show. A TA contraction now occurs, the peak of which occurs another 20–25 ms after the activation Alipour-Haghighi et al., 1987 . This is shown in Fig. 2 f . Vocal-fold strain is now reduced Fig. 2 g , with a concomitant increase in the length of the CT muscle and a receptor activation Fig. 2 h . The reflex loop is engaged once more, resulting in another delay for sensory-motor in-

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FIG. 2. Time course of efferent and afferent stimuli, and muscle activation. tegration Fig. 2

FIG. 2. Time course of efferent and afferent stimuli, and muscle activation.

tegration Fig. 2 i and another CT contraction Fig. 2 j . The complete cycle, from the peak of CT contraction to the peak of CT contraction, has a period of about 170 ms, yield- ing a vibrato frequency of about 6 Hz.

III. DYNAMICS OF THE MUSCLES AND OTHER SOFT TISSUES

Mathematically, the model begins by letting both muscles be represented mechanically by a Kelvin model McMahon, 1984, p. 136 , as shown in Fig. 3. This model has a series spring k s , a parallel spring k p , a damper d, and an internal contractile stress i in the case of muscle . The onset of the internal contractile stress is time delayed by a first-order differential equation Stein and Oguzto ¨ reli, 1975

1

where the ‘‘dot-over’’ notation indicates time differentiation, t a is the activation time constant, and a is the fully devel- oped active stress.

˙ i a i /t a i 1,2,

J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002

A second differential equation for the muscle model is obtained by writing Newton’s law for the internal left nodal point indicated in Fig. 3

S i k s L o i dL o

˙

i 0,

2

3 S i k s L o i dL o ˙ i 0, 2 FIG. 3.

FIG. 3. Kelvin muscle model for twitch and tetanus force computation.

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TABLE I. Biomechanical constants of the cricothyroid muscle.

Symbol

Value

Resting length Cross-sectional area Mass Maximum active stress Activation time Series contraction time

L o

S

M

am

t a

t s

13.8 mm 73.8 mm 2 0.9423 g 89 kPa 0.01 s 0.090 s

and a nondifferential equation is obtained by writing New- ton’s law for the external right nodal point

3

where S is the cross-sectional area of the muscle, L o is the rest length, i is the internal sarcomere strain, is the ex- ternal muscle strain, and F is the external load force. Equa- tion 2 , the nondifferential equation, is now solved for i and substituted into Eq. 3 to yield

F k p L o k s L o i 0,

S i F k p L o

d

k s

F d k p k s L o ˙ 0.

˙

k s

4

To simplify the model and capture only its essence in this first exposition of vibrato, the passive tissue force k p L o will be neglected. This passive force is usually an order of magnitude smaller than the active force Alipour and Titze, 1999 except for high strains 30%–50% of rest length . We will keep the strains below 10% in our simulations. Further- more, the strain rate is low in vibrato, which allows the ˙ term in Eq. 3 to be neglected also in comparison to the active fiber tension S i . With these simplifications, Eq. 3 reduces to

˙

F S i F /t s ,

where

5

t s

d

k s

.

6

Equations 1 and 4 develop the load force in each muscle, based on activation delay and active stress in the fibers. The series contraction time t s of the sarcomere is part of the overall delay of response of the muscle system Stein and Oguzto ¨ reli, 1975 . Tables I and II show measured values of the parameters for the CT and TA muscles, respectively. These values were obtained in our laboratory over a period of more than a decade Alipour-Haghighi, Titze, and Durham, 1987; Perlman and Alipour-Haghighi, 1988; Alipour-Haghighi, Titze, and Perlman, 1989; Alipour, Perlman, and Titze, 1991; Alipour and Titze, 1999 . The properties were obtained from a canine model, however, and must be regarded as approximations to human tissues. The fully developed active stress function a in Eq. 1 is generated for each muscle as

7

where a(t) is the muscle activation ranging from 0 to 1 and am is the maximum active force achievable in the muscle under isometric conditions Tables I and II . Usually this maximum active force varies with muscle strain , but to

a a t am ,

2276 J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002

TABLE II. Biomechanical constants of the thyroarytenoid muscle.

Symbol

Value

Resting length Cross-sectional area Mass Maximum active stress Activation time Series contraction time

L o

S

M

am

t a

t s

18.3 mm 40.9 mm 2 0.8232 g 105 kPa 0.01 s 0.044 s

keep the model simple we will keep it a constant value, which is justifiable because strain variations are small in vi- brato.

IV. DYNAMICS OF THE CARTILAGE FRAMEWORK

The differential equations of motion for translation and rotation of the cricoid cartilage in relation to the thyroid cartilage were developed previously Titze, 1996 . These equations are rewritten here for completeness. For translation

and rotation around the cricothyroid joint Fig. 4

¨ 1

M

˙

cos F CT F TA k t t t ,

8

 

1

¨

˙

I wF CT hF TA k r t r ,

9

where F CT is the load force generated by the CT muscle, F TA is the load force generated by the TA muscle, cos 0.76 is the direction cosine between CT and TA lines of action, w 0.011 m is the moment arm for CT force in CT joint rota- tion, h 0.016 m is the moment arm for TA force in CT joint rotation, M 0.01 kg is the mass of cricoid and arytenoid cartilages translating as a unit relative to the thyroid carti- lage , I 10 5 kg m 2 moment of inertia of cricoid and arytenoid cartilages rotating as a unit around the CT joint, k t is the stiffness of CT joint in translation defined below , k r is the torsional stiffness of the CT joint in rotation defined below , t t 0.010 s is the time constant for translation, speci- fying viscous damping, and t r 0.010 s is the time constant for CT joint rotation, specifying viscous damping. The strains 1 and 2 of the CT and TA muscles, respec- tively, are related to and as follows:

10

11

where L 01 and L 02 are the rest lengths of the muscles. These are the strains used for the receptor pathways in Fig. 1. The translational stiffness k t in Eq. 8 has been mea- sured as a nonlinear function of strain by Vilkman et al. 1987 . We give the following approximation to their data:

12

Similarly, the rotational stiffness has been measured by Coo- per et al. 1993 , approximated here as

13

The nonlinear nature of these stiffnesses provides the limit cycle for oscillation in vibrato. If the stiffnesses were linear,

1 w /cos /L 01 ,

2 h /L 02 ,

k t 1000 10 5 /L 01 2 N/m.

k r 0.1 10 h /L 01 2 N-m/radian.

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FIG. 4. Laryngeal cartilages in a translation and b rotation. underdamped oscillation would continue to

FIG. 4. Laryngeal cartilages in a translation and b rotation.

underdamped oscillation would continue to grow beyond bound.

V. DYNAMICS OF SENSORY FEEDBACK

Feedback from the sensory organs is modeled by letting the modulated muscle activities be

14

a TA t A TA t g 2 2 t 2 0.03 ˙ 2 t 2 , 15

where all quantities are as previously defined. A CT (t) and A TA (t) are taken as a constant tetanic activation with su- perimposed low-frequency noise that simulates physiologic muscle tremor. The coefficient 0.03 is chosen to weight the strain and strain-rate dependence of the delayed feedback

a CT t A CT t g 1 1 t 1 0.03

˙

1 t 1 ,

J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002

, J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002 FIG. 5. Experimental

FIG. 5. Experimental setup for mechanical stimulation.

equally, since for sinusoidal strain ˙ and is about 30 rad/s for a 5–6-Hz vibrato rate. This completes the mathematical description of the re- flex resonance model. Parameters that are of primary interest in this paper are the reflex delay times 1 and 2 and the reflex gains g 1 and g 2 .

VI. EXPERIMENTS TO DETERMINE REFLEX GAINS AND DELAYS

Two separate experiments are described in this section. The first experiment involved mechanical stimulation to the larynx to determine the reflex latency. The second experi- ment involved electromyographic EMG recordings to de- termine the sharpness of the reflex resonance, which we claim is an indirect measure of the reflex gain.

A. Mechanical stimulation

An experiment was conducted to measure the reflex de- lay associated with mechanical perturbation of vocal-fold length. Two nonsingers, both adult males, served as subjects. EMG electrodes were inserted into both CT and TA muscles to monitor their laryngeal reflexes. A mechanical stimulator was designed in the form of a servo-controlled rod that could push against the thyroid cartilage prominence Adam’s apple as shown in Fig. 5. The subject sat in a chair in an upright position. His head was secured in place by a head- rest. The servo-controlled stimulator was mounted on a rig attached to the chair. The rod had several mm of electroni- cally controllable travel distance after it had been fixed in place, in near-contact with the thyroid cartilage. Thus, the experimenter could adjust the neutral position as ‘‘light con- tact,’’ ‘‘near-contact,’’ or ‘‘pressured contact.’’ Because the thyroid prominence is rounded, and because the endplate of the rod did not have an ideal cup shape to fit over all the subjects’ thyroid prominences, there was occa-

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FIG. 6. Reflex latencies for mechanical stimulation. sionally some slippage of the rod off-center. This

FIG. 6. Reflex latencies for mechanical stimulation.

sionally some slippage of the rod off-center. This was noted

in

the experiment, and the data were accepted with caution,

or

rejected if the slippage was too severe. Once the neutral position was adjusted, the rod displace-

ment was varied in single-pulse or square-wave fashion with

a preset displacement amplitude and frequency for the

square wave . A decrease in vocal-fold strain was achieved by pushing against the thyroid cartilage. According to our model, this should activate the CT receptors spindles or joint receptors and produce an increase in the motor activa- tion a CT to the CT muscle. The objective was to measure the reflex latency 1 . Figure 6 shows results for subject S1. Transducer dis- placement and force are shown at the bottom upward dis- placement means a push toward the cartilage, with an ex- pected negative vocal-fold strain . The displacement amplitude was 2 mm, but there was no knowledge of how much shortening of the vocal-fold this actually produced. The entire larynx was obviously pushed rostrally, which meant that the arytenoid cartilages may have moved together with the thyroid cartilage to produce a lesser change in vocal-fold length. Nevertheless, some reduction in length was expected. The EMG responses of the right CT muscle R CT EMG and the left CT muscle L CT EMG are shown in the top two traces in Fig. 6. Note that the reflex latency between the maximum velocity of movement time 0.00 and the peak of the EMG increase is about 40 ms. Results for the second subject were similar, with the reflex latency being about 44 ms from the maximum move- ment velocity to the peak of the EMG increase. Both CT muscles showed an increase in activity, but the TA muscles did not. This average reflex latency of about 42 ms for the two subjects was built into our reflex resonance model as the variable 1 . We had no way of pulling on the cartilage to elongate the vocal-folds and obtain a TA reflexive contrac- tion. Hence, 2 was chosen to be the same as 1 for lack of better data. If the two time constants were in fact different, a slight asymmetry would be expected in the vibrato cycle, and the overall vibrato rate would increase or decrease slightly.

2278 J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002

2278 J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002 FIG. 7. Resonance

FIG. 7. Resonance curves amplitude of F o modulation in Hz for: CT stimulation and no natural vibrato data points ; no stimulation and no natu- ral vibrato curves without data points .

B. Electrical stimulation

Electrical muscle stimulation experiments were con- ducted on four new subjects, one soprano trained in classical and theatre styles more than 10 years of private training , one mezzo-soprano trained in classical music more than 5 years of private training , one untrained female pop singer no private lessons , and one female nonsinger. New sub- jects were used because repeated electrode insertion in close time intervals is not recommended for a given subject, espe- cially not for singers. Electrical stimulation was applied to the CT muscle during phonation with bipolar hooked-wire electrodes, the same electrodes normally used to record EMG signals Titze et al., 1994 . The resonance condition of the reflex loops was investigated by repeated pulse stimula- tion of the CT at different frequencies during phonation. Ac- cording to our model, this would involve the TA reflex as well as the CT reflex. Those subjects who had a natural vi- brato were asked to sustain the vowels vibrato-free. Our hy- pothesis was that if the same pulse current and duration could produce a larger F o swing at one frequency than all others, then a resonance of the reflex system must exist. Fig- ure 7 shows the results in the form of amplitude spectra of the F o contour for the four female subjects. The curves with- out data points show the spectrum of physiologic tremor without any stimulation, whereas the curves with data points are for stimulation at the frequencies shown by the points. With stimulation, we see a tuning curve with a 5-Hz reso- nance frequency for the two trained singers parts a and b and about 6 Hz for the untrained singer part c . For the one nonsinger part d , no clear tuning is evident be- cause a heightened response in the 4–6-Hz region was present without stimulation. The subject was quite nervous about the procedure, suggesting that an anxiety tremor may have caused this response. The singers, on the other hand, showed no remarkable peaks without stimulation. This re- sult, although poor in sample size, begins to confirm the

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FIG. 8. Resonance curves amplitude of F o modulation in Hz for CT stimu- lation,

FIG. 8. Resonance curves amplitude of F o modulation in Hz for CT stimu- lation, with and without natural vibrato. Lines with diamond-shaped data points are for the vibrato case, while lines with the solid black circles are for the no vibrato case.

hypothesis that singing training may heighten the reflex gains and establish a reflex resonance. It is important to note that this happened when the singers were deliberately sing- ing a straight tone vibrato-free . When the singers allowed their vibrato to be present, the resonance was sharpened Fig. 8 , especially for the trained singer in part a . The peak rose to 7 Hz 14 Hz peak to peak and the bandwidth decreased, although exact measurement of the bandwidth was difficult without a finer grid of stimu- lation frequencies. Such a grid would require a new protocol with new subjects, due to fatiguing factors. A final data set for the four female subjects Fig. 9

A final data set for the four female subjects Fig. 9 FIG. 9. Resonance curves amplitude

FIG. 9. Resonance curves amplitude of F o modulation in Hz for CT stimu- lation at three frequencies, no natural vibrato. Open circles represent F o 196 Hz, solid black circles represent F o 330 Hz, and asterisks represent F o 440 Hz.

J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002

shows the response curves at different singing pitches: low, mid, and high. The corresponding F o values were 196 Hz G3 , 330 Hz E4 , and 440 Hz A4 . Only the second trained singer part b showed a remarkable difference in response to stimulation at different pitches. Lower pitches gave greater response. This subject was a high soprano who probably only engaged her TA muscle at low pitches, thereby producing a better agonist–antagonist reflex loop. The first trained singer Fig. 9 a was a mezzo-soprano who tended to maintain the TA muscle engaged throughout the pitches, which may have resulted in the more uniform patterns. In hindsight, it may have been better to have the subjects per- form at physiologically equivalent pitches, based on their overall voice-range profile, but given the invasive nature of the experiment it was impossible to repeat the protocol. Also, the voice-range profile would have added to the vocal load, which was already quite heavy.

C. Computer simulation of vibrato

Equations 1 15 were programed in MATLAB, using a fourth-order Runge–Kutta technique to solve the differential equations. The computation began by coding the intended muscle memory with a constant level of activation, 20% for CT and 20% for TA, superimposed by either a pulse stimulus or by low-pass-filtered noise in the 0–15-Hz range. That pro- duced the subcortical activities A CT and A TA in Fig. 1. The response to the pulse stimulus is shown in Fig. 10. This figure is essentially a quantification of the hypothetical set of events outlined in Fig. 2. Note the twitch force in the CT following a single pulse activation top two traces . The pulse was initiated at 0.5 s to allow the tetanic muscle con- tractions to bring the system to equilibrium in the first half- second. In the third trace from the top, we see the vocal-fold strain exhibiting damped oscillation, a typical response of a natural resonator. The frequency is about 6.5 Hz and the strain variation is less than 0.05. The first rise after 0.5 s corresponds to the strain rise hypothesized in Fig. 1 c . Note also that the reflexive TA activity fourth trace from top is delayed about 80 ms in reference to the pulse, which was hypothesized in Fig. 1 e . Figure 10 is completed by showing the TA force and the F o contour in the bottom two traces. Note the further delay between the peaks of TA activity and TA force in the initial excursions. The F o contour was computed with the simple vibrating string formula

F o

2L o F TA

1

S ,

16

where is the tissue density (1140 kg/m 3 ), and L o and S are the TA muscle length and cross-sectional area as previously defined Table II . With this formula, the F o modulation am- plitude in Fig. 10 is about 10 Hz initially, damping out with successive cycles. The reflex gains g 1 and g 2 were chosen to be 1.5 in Eqs. 14 and 15 , and the neural reflex delays 1 and 2 were set at 45 ms. Figure 11 shows the effect of varying reflex gain. An FFT analysis was done on the F o impulse responses bottom trace of Fig. 10 for g 1 g 2 1.0, 1.5, and 2.0. The spectra

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FIG. 10. Simulation of an impulse response of the com- puter model of vocal vibrato.

FIG. 10. Simulation of an impulse response of the com- puter model of vocal vibrato. The reflex gain was set to 1.5.

were normalized to the peak values to show the slight shift in the vibrato frequency with gain. The frequency increases by about 0.5 Hz from 6.0 to 6.5 Hz as the gain increases from 1.0 to 2.0. But, much more dramatically, the bandwidth is lowered by increasing the gain. Thus, the tuning to a single vibrato frequency is very sharp for high gain. To put the magnitude of the gain in perspective, a gain of 1.0 means that, according to Eqs. 14 and 15 , the feedback modula- tion activity is on the order of 0.02 the value of the peak strain superimposed on a background tetanic muscle activity of 0.2. This is a 10% feedback ratio, which the spindles and the sensory-motor synapses have to produce to achieve the oscillation. It should be pointed out that the normalization of the spectra in Fig. 11 does not give the true picture of increased gain. If normalization were to the noise floor, the gain 2.0 curve would rise 30 dB above the gain 1.0 curve, a dra- matic increase in F o variation. A lesser, but nevertheless dra- matic, increase was seen in Fig. 8 a for one trained singer when she switched her vibrato on. We reason, therefore, that the reflex gain does not have to change much only a few percent to get a substantial increase in vibrato extent. The second set of simulations was done with low-pass- filtered noise 15 Hz cutoff to simulate physiologic tremor activity. The result is shown in Fig. 12. The top trace shows constant CT activity (a ct 0.2) for the first 0.5 s, followed by low-frequency tremorous activity for the next second. Self-sustained oscillation is seen in the third trace, labeled strain, but the oscillation is not quite sinusoidal. The 6-Hz dominant frequency is clearly visible, however. The gain was set at 1.5, the same as for the pulse excitation in Fig. 10. Note that F o modulations in Fig. 12 bottom trace have an amplitude of about 10 Hz, which is 7% of the mean F o of 150 Hz. Although this is a little larger than most natural vibrato extents, it is not unrealistic in relation to what trained singer 1 produced in Fig. 8. Parenthetically, we note that white noise, which was also tried as an excitation, produced smaller F o amplitudes than the colored low-pass noise. Fig-

2280 J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002

ure 13 shows the spectrum of the F o contour with 0–15-Hz tremor-like noise excitation. The 6-Hz reflex tuning is clearly visible in the low-frequency noise.

VII. DISCUSSION

We now return to the ten observations about vocal vi- brato that were listed in the Introduction. The first observa- tion, that vibrato extent is more controllable by a singer than vibrato frequency, is confirmed by our results. When the singers changed voluntarily from vibrato to no-vibrato con- ditions, the magnitude of the F o modulation decreased, but the frequency did not change appreciably. Since vibrato ex- tent is controlled by the reflex gains in our model, we sug- gest that singers adjust reflex gains rather than reflex delays when they change from straight tone to vibrato. The reflex delays are less controllable on a moment-to-moment basis, because they involve neural conduction times, muscle acti-

because they involve neural conduction times, muscle acti- FIG. 11. Frequency spectra of the F o

FIG. 11. Frequency spectra of the F o contours after pulse excitation, for three values of reflex gain. The sampling frequency was 1 kHz and the analysis window was 10 s. The spectra are normalized to their peaks.

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FIG. 12. Simulation of vibrato with tremor-like 0–15- Hz noise excitation. The reflex gain was

FIG. 12. Simulation of vibrato with tremor-like 0–15- Hz noise excitation. The reflex gain was 1.5.

vation times, and muscle twitch contraction time, all of which are firm-wired in the neuromuscular system. The second observation, that many children and some adults sing vibrato-free, is also likely to be explained by reflex gains. In children, the thyroarytenoid muscle develops late Hirano and Sato, 1993 , which means that the spindles may not be in place to activate a vocal-fold stretch reflex. In some adults, there is not much length change at all when F o is varied Nishizawa et al., 1988 . In other words, the CT joint is stiff, or the spaces between the cartilages are small. This may reduce the effective feedback. The third observation, that some geriatric or poorly con- ditioned vocalists have a slow and wide vibrato a wobble , may be explainable on the basis of increased reflex delays. It is well known that nerve conduction velocities slow with age Chase et al., 1992; Rosenberg et al., 1989; Xi et al., 1999 and that muscle activation and contraction times increase with age. Poor muscle conditioning, regardless of age, also increases the contraction times slower muscle response . Thus, it is not surprising to see a 1–2-Hz reduction in vibrato frequency with age. A wobble can often be corrected by ton- ing the laryngeal muscles to increase contraction times . Also, by singing softly at the extremes of the pitch range, less bulk of the TA muscle is involved in vibration, which is likely to reduce the response time. The fourth observation, that muscularly hyperactive tense vocalists sometimes have an excessively fast vibrato a bleat , may also be explainable on the basis of reflex la- tencies. Muscles that are already primed potentiated re- spond quicker in a twitch mode than those that are somewhat relaxed. Thus, vocal relaxation exercises with the mental image of letting the tone flow easily rather than pushing it could understandably reduce the vibrato frequency. But, the process of change is slow, with significant results often being achieved only over several months of exercising. The fifth observation, that training reduces the variabil- ity increases regularity in vibrato rate and extent, may be explained by increased reflex gains, i.e., by a sharper tuning

J. Acoust. Soc. Am., Vol. 111, No. 5, Pt. 1, May 2002

curve. The tremor frequencies are then filtered more effec- tively to define a narrow band around 5–6 Hz, as was shown with our model. The sixth observation, that violin, brass, and woodwind vibrato are similar to vocal vibrato, is explainable if we as- sume that there are always two agonist–antagonist muscles that are involved in similar reflex action. These muscles could be in the hand and fingers as in violin playing , in the articulatory system, or even in the respiratory system. A res- piratory vibrato, however, tends to be slower around 4 Hz or less because of the slower response of the muscles around the abdomen, diaphragm, and ribcage. Some mechanical loading may also affect the vibrato frequency. In our model, the mechanical natural frequency for cricothyroid rotation was 17 Hz based on values of the moment of inertia and rotational stiffness , and the natural frequency of cricothy- roid translation was 50 Hz based on cricoid mass and joint stiffness . These frequencies are too high to mass load the

. These frequencies are too high to mass load the FIG. 13. Frequency spectrum of F

FIG. 13. Frequency spectrum of F o contour with tremor-like 0–15-Hz noise excitation. The reflex gain was 1.5.

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reflex resonance. But, for larger structures, mechanical load- ing may be important. The seventh observation, that some pathological vocal tremors are also around 5–6 Hz Koda and Ludlow, 1992 , suggests that perhaps reflex gains can become too large and no longer able to be inhibited voluntarily. The reflex oscilla- tor is highly underdamped, growing in oscillation amplitude to reach a limit cycle largely determined by structural con- straints. This would also explain why boundary structures jaw, tongue, pharynx are sometimes engaged in the overall tremulous activity. The eighth observation, that vibrato frequency increases at the end of a note Prame, 1994, 1997 , may mean that twitch contraction times vary with the degree of muscle length and activation. Perlman and Alipour 1988 showed that twitch contraction times increased with vocal-fold length. As the vocal-folds abduct, the TA muscle is elon- gated. This may increase the contraction to raise the vibrato frequency, but whether or not it can account for a difference of about 1.0 Hz is not clear. Other explanations should be sought as well. The ninth observation, that natural vibrato is more easily achieved in the midrange of F o than at the extremes, may simply mean that the two agonist–antagonist muscles work with nearly equal strains, thereby providing alternating and nearly similar reflex activations, rather than one muscle be- ing highly strained and the other being lax which provides unequal spindle activation . The tenth observation, that the natural singer’s vibrato can be entrained by an outside stimulus Titze et al., 1994 , has not been a target of investigation here. The auditory re- flex has also not yet been included in the current model; it is conceivable that an auditory stimulus from another singer could override the central tremor oscillators and pull the natural vibrato slightly away from its natural resonance, but this awaits further study.

ACKNOWLEDGMENTS

This study was supported by Grant Number R01 DC 04347-01. We are highly appreciative of Jeannie Lovetry, who assisted in this study with funds obtained through a Van Lawrence fellowship from the Voice Foundation. We also thank Professor Charles Larson of Northwestern University, who was instrumental in part of the data collection and de- sign of the mechanical driver for the larynx.

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