"Chaos" is a term that describes pseudorandom behavior generated by a system that is both deterministic and nonlinear. Methods based on nonlinear dynamics can be used to quantify chaos and irregularity in vocal fold vibration. Studies have suggested that pathologies such as laryngeal paralysis, vocal polyps, and vocal nodules might exhibit chaotic behaviors.
"Chaos" is a term that describes pseudorandom behavior generated by a system that is both deterministic and nonlinear. Methods based on nonlinear dynamics can be used to quantify chaos and irregularity in vocal fold vibration. Studies have suggested that pathologies such as laryngeal paralysis, vocal polyps, and vocal nodules might exhibit chaotic behaviors.
"Chaos" is a term that describes pseudorandom behavior generated by a system that is both deterministic and nonlinear. Methods based on nonlinear dynamics can be used to quantify chaos and irregularity in vocal fold vibration. Studies have suggested that pathologies such as laryngeal paralysis, vocal polyps, and vocal nodules might exhibit chaotic behaviors.
Madison, Wisconsin Summary: Chaos has been observed in turbulence, chemical reactions, nonlin- ear circuits, the solar system, biological populations, andseems tobe anessential aspect of most physical systems. Chaos may also be central to the interpretation of irregularity in voice disorders. This presentation will summarize the results from a series of our recent studies. These studies have demonstrated the prescence of chaos in computer models of vocal folds, experiments with excised larynges, and human voices. Methods based on nonlinear dynamics can be used to quantify chaos and irregularity in vocal fold vibration. Studies have suggested that disordered voices from laryngeal pathologies such as laryngeal paralysis, vocal polyps, and vocal nodules might exhibit chaotic behaviors. Conventional parameters, such as jitter and shimmer, may be unreli- able for analysis of periodic and chaotic voice signals. Nonlinear dynamic methods, however, have differentiated between normal and pathological phon- ations and can describe the aperiodic or chaotic voice. Chaos theory and nonlinear dynamics can enchance our understanding and therefore our assess- ment of pathological phonation. Key Words: ChaosNonlinear dynamic methodsVocal fold model Voice analysis. INTRODUCTION Chaos is a term that describes pseudorandom behavior generated by a system that is both deter- ministic and nonlinear. Although chaos was once thought to be unique, it has now been widely ob- served, such as in turbulence, chemical reactions, nonlinear circuits, the solar system, and biological Accepted for publication January 5, 2005. From the Department of Surgery, Division of Otolaryngology Head and Neck Surgery, University of Wisconsin Medical School, Madison, WI 53792-7375. E-mail: jiang@surgery.wisc. edu Supported by the National Institute of Deafness and other Communication Disorders under National Institutes of Health grants 1-RO1DC006019 and 1-RO1DC05522. Journal of Voice, Vol. 20, No. 1, pp. 217 0892-1997/$32.00 2006 The Voice Foundation doi:10.1016/j.jvoice.2005.01.001 2 populations. 1 Recent studies in neurology and cardi- ology suggest that chaotic activity is an important aspect of physiologic systems. 2 An example of phys- iologic chaos was presented in the in vitro studies of heart cells fromembryonic chicks, 3 in which electric shocks delivered to heart cells resulted in period- doubling bifurcations and irregular dynamics. The output of a chaotic system is unpredictable and extremely sensitive to slight differences in initial conditions. However, methods based on nonlinear dynamics, including general dimension (Hausdorff dimension, information dimension, correlation dimension, etc.), entropy (Kolmogrov entropy, second-order entropy, etc.), and Lyapunov expo- nents, enable us to quantitatively describe chaotic behavior. 1,4 Investigations of chaotic activities in physiologic systems suggest that changes in nonlinear dynamic measures may indicate states of pathophysiological dysfunction. Poon and Merrill, 5 CHAOS IN VOICE 3 for example, found that chaotic activity decreased in electrocardiogram (ECG) signals from patients with congestive heart failure. Hornero et al 6 found that the electroencephalogram (EEG) signals gener- ated by schizophrenic patients had a signicantly lower correlation dimension than the EEG signals of normal subjects. These examples suggest that chaos theory and nonlinear dynamic methods might potentially be applied to diagnose physiologi- cal disorders and evaluate the effects of clinical treatments. Over the last two decades, observations in com- puter models of the vocal folds, 717 experiments with excised larynges, 1820 and nonlinear dynamic analy- sis of human voices 2129 have established the exis- tence of chaos in human voice production. As noted by many researchers, the nonlinearities of the voice source mechanisms (eg, the nonlinear pressure-ow relation in the glottis, the nonlinear stress-strain curves of vocal fold tissues, and the nonlinearities associated with vocal fold collision) make this devel- opment unsurprising. Titze et al 24 originally sug- gested how to improve our understanding of voice disorders with nonlinear dynamic concepts and anal- ysis methods. Since then, researchers have applied these new tools to studying abnormal conditions associated with laryngeal pathologies, 8,11,16,25,3034 to differentiate normal and pathologic voices and diagnose pathologies, 3540 and to assess the effects of clinical treatments. 41 These studies are promising, although much development is still needed for prac- tical methods. Some traditional voice analysis meth- ods, such as jitter and shimmer, may be unreliable for analyzing aperiodic voices. 30,4244 Nonlinear dynamic methods provide information complemen- tary and nonredundant to existing analysis meth- ods. 25,37,40 Thus, nonlinear dynamic methods could provide more information to clinicians. In this article, we review our recent work on the application of chaos theory and nonlinear dynamic methods to the study of voices, focusing on studies with computer vocal fold models, excised laryn- ges, and human voices. The work of other research- ers is also briey reviewed. The purpose of this article is to stimulate the development of clinically valuable analysis methods that can be applied to quantify chaotic laryngeal activity and to assess Journal of Voice, Vol. 20, No. 1, 2006 treatment effects of laryngeal pathologies. The em- phasis is on applying chaos theory and nonlinear dynamic methods to achieve this goal. WHY NONLINEAR DYNAMIC ANALYSIS? Titze 30 has qualitatively classied voice signals into type 1, type 2, and type 3 signals. Type 1 signals are nearly periodic, type 2 signals contain strong modulations or subharmonics, and type 3 sig- nals are irregular and aperiodic. The typical wave- forms of the three types of signals are shown in Figure 1, 34 where the sampling rate is 25 kHz, the fundamental frequency f 0 1/T, and A, B, and C correspond to the waveforms of the type 1, 2, and 3 signals, respectively. Usually, the complexity of a voice signal affects the applicability of traditional analysis methods. It has been suggested that jitter and shimmer, which are two acoustic perturbation measures that have been traditionally used by re- searchers, are appropriate only for nearly periodic type 1 signals. Jitter is a measure of short-term (cycle-to-cycle) variation in the fundamental fre- quency of a voice signal, and shimmer is a measure of short-term (cycle-to-cycle) variation in the ampli- tude of a voice signal. Perturbation measures such as jitter and shimmer presuppose, by denition, near periodicity, and thus their usefulness may break down for type 2 and type 3 signals. Studies examin- ing the reliability and applicability of jitter and shim- mer have found large variances and poor reliability FIGURE 1. The typical waveforms of type 1, type 2, and type 3 voice signals. JACK J. JIANG ET AL 4 when analyzing disordered or aperiodic voices. 30,4244 Spectrographic display and perceptual analysis have been recommended for type 2 and type 3 signals, respectively. 30,44 Although perceptual evaluation of vocal function is simple, the inherent subjectivity of perceptual judgments makes them potentially un- reliable as well as difcult to quantify. 45,46 Factors that contribute to the inconsistencies of perceptual evaluation include different internal standards be- tween the raters of a voice signal and differences in how listeners focus their attention on the various aspects of voice. 47 In addition, both perceptual eval- uation and spectrographic display may fail to quanti- tatively detect subtle changes in vocal function. Because traditional voice analysis methods are lim- ited, complementary objective measures that analyze both nearly periodic and aperiodic voices are desirable. Nonlinear dynamic methods, including Poincare map, fractal dimension, correlation dimension, Kol- mogorov entropy, and Lyapunov exponents, can ana- lyze irregular or chaotic activities. 1,4,48 We will briey describe three such methods that have ana- lyzed voices: the correlation dimension, the Lyapu- nov exponents, and the Kolmogorov entropy. To understand these analysis methods, the concept of a phase space needs to be described. A phase space is a space dened by multiple dynamic variables composed of positions and velocities. The vibra- tions of a dynamical system such as the vocal folds can be shown as a trajectory in phase space with time evolution. The trajectory in phase space qualitatively shows the dynamics of a system: Periodic vibrations produce a closed trajectory, whereas aperiodic vibra- tions produce an irregular trajectory. When multiple dynamic variables cannot be assessed, it is useful to reconstruct the phase space of a voice signal by plotting a single time series x(t i ), t i t 0 it, (i 1,2,,N), which is sampled at the time interval , against itself at some time delay or lag. 4,49 We can create the reconstructed phase space with the fol- lowing m-dimensional time delay vector, X(t){x(t),x(t),,x(t(m1))}, where mis the embedding dimension and is the time delay. When m 2D 1 (where D is the Hausdorff dimension), the reconstructed phase space is topologically equiv- alent to the original phase space. Because of the nite length and nite precision of voice data, the Journal of Voice, Vol. 20, No. 1, 2006 time delay is an important parameter in the recon- struction of a phase space. If is too small, the lagged variables are strongly correlated such that the trajectory in the reconstructed phase space is stretched around a diagonal line. On the other hand, if is too large, the trajectory in the reconstructed phase space is characterized by self-intersection. Proper choice of the time delay yields an optimal phase space reconstruction. The time delay can be estimated with the mutual information method proposed by Fraser and Swinney. 50 Mutual informa- tion measures the general dependence of two vari- ables. Fraser and Swinney 50 found that the rst minimum value in the curve of mutual information versus time delay provides an effective criterion for choosing the proper time delay , which will ensure that the variable and lagged variables are gener- ally independent. The correlation dimension D 2 , which was pro- posed by Grassberger and Procaccia, 51 is a geometric measure of a trajectory in phase space that describes how strongly two points on the trajectory are corre- lated. It has been widely used by researchers in experiments because of its simplicity and fast convergence in numerical calculation, as well as its ability to describe irregular phenomena. The correla- tion dimension quanties the complexity or irregu- larity of a trajectory in phase space, which can be classied as a zero-dimensional xed point (static states), a one-dimensional limit cycle (periodic os- cillations), a two-dimensional quasi-periodic torus (superposition of two or more oscillations with no rationally dependent frequencies), or a fractal- dimensional chaotic trajectory (aperiodic oscilla- tions). A system with a higher correlation dimension may require more variables to describe its behavior. With the correlation dimension, chaos can be distin- guished from random white noise: The estimate of D 2 of white noise does not converge with the in- crease of the embedding dimension m, whereas the estimate of D 2 of a chaotic system converges to a nite value. Although Lyapunov exponents require complex numerical algorithms, they have proven to be one of the most effective descriptors of chaos. Lyapunov exponents are related to the average rate of exponential divergence or convergence of neigh- boring orbits in phase space. Generally, a system containing at least one positive Lyapunov exponent CHAOS IN VOICE 5 is dened as chaotic, whereas a system with no positive exponent is regular. Asystemwith a positive Lyapunov exponent shows local instabilities and extreme sensitivity to initial conditions. In other words, any slight change in state will be exponentially amplied, which results in a totally different output. Kolmogorov entropy quanties the rate of loss of information about the state of a dynamic system as it evolves over time. For regular behaviors (static states, periodic oscillations, and quasi-periodic os- cillations), Kolmogorov entropy is equal to zero. For chaotic systems with nite degrees of freedom, Kolmogorov entropy is nite. Kolmogorov entropy approaches innity for true randombehavior. Thus, a nite and positive second-order entropy value (the lower bound of Kolmogorov entropy) provides a sufcient condition for chaos. 52 We will briey describe the procedures that calcu- late correlation dimension, Kolmogorov entropy, and Lyapunov exponents. Readers interested in de- tailed descriptions of calculation procedures should refer to the literature. 1,4,8,10,14,20,21,2441,4852 For a time series x(t i ), we reconstructed a m-dimensional delay-coordinate phase space X i {x( t i ),x( t i ),, x( t i (m1))} with the time delay technique, where m was determined according to the embedding theo- rem and the time delay was estimated with the mutual information method proposed by Fraser and Swinney. 50 After reconstructing the phase space of a time series, we used the GrassbergerProcaccia algorithm 51 with the Theiler 53 improvement to calcu- late the correlation integral C(r), where r is the radius around X i . The correlation integral C(r) measures the number of distances between points in the recon- structed phase space that are smaller than the radius r. For small r, C(r) shows a power lawbehavior C(r) r D2 e m K2 which reveals the geometrical scaling property of the trajectory in phase space. 51 Based on C(r), we estimated the correlation dimension D 2 in the scaling region of the radius r with the increase of the embedding dimension m. The estimate of correlation dimension can be obtained when the em- bedding dimension m is sufciently large. Figure 2A shows the reconstructed phase space of the type 3 signal in Figure 1, where t 1/f s , the sampling rate f s 25 kHz, and the proper time delay 11 t was obtained with the mutual information method. Journal of Voice, Vol. 20, No. 1, 2006 FIGURE 2. A. The reconstructed phase space of the type 3 signal, where t 1/ f s and f s 25 kHz. B. The estimated dimension versus r, in which the curves from top to bottom correspond to m 1,2,,10, respectively. Figure 2B shows the curves of the estimated dimen- sion versus r. Despite the irregular shape of the reconstructed phase space, the estimated correlation dimension converges to 3.560.04 within the scal- ing region 13.6 r 14, when m increases from 1 to 10 (see Figure 2B). Similar to the correlation dimension D 2 , second-order entropy K 2 was esti- mated in the scaling region of the radius r with the increase of the embedding dimension m. 52 We used the method of Holzfuss and Lauterborn 54 to calculate the Lyapunov exponents of a time series. To investigate the variability of jitter, shimmer, and correlation dimension analysis over time, we used a running window to analyze 11 consecutive JACK J. JIANG ET AL 6 400-ms voice segments selected from a nearly peri- odic signal and 11 consecutive 400-ms voice seg- ments selected from an aperiodic signal. The nearly periodic signal was producedbyanormal subject, and the aperiodic signal was produced by a patient with a vocal polyp. The time shift between two consecu- tive segments was 20 ms. Jitter and shimmer were estimated with the Multi-Dimensional Voice Pro- gram (MDVP; Kay Elemetrics Corporation, Lincoln Park, NJ). Figure 3 shows the variability of jitter, shimmer, and correlation dimension over time for the nearly periodic and aperiodic signal, where curves I, II, III, IV, V, and VI correspond to D 2 of the periodic voice, D 2 of the aperiodic voice, jitter of the periodic voice, jitter of the aperiodic voice, shimmer of the periodic voice, and shimmer of the aperiodic voice, respectively. Jitter, shimmer, and correlation dimension provide stable analyses for the nearly periodic type 1 signal. However, for the aperiodic type 3 signal, jitter and shimmer show large variances and thus poor reliability, whereas the correlation dimension has a comparatively small variance, which demonstrates its reliability for analysis of disordered or aperiodic voices. 55 This example suggests that nonlinear dynamic analysis methods represent more useful descriptors of irregu- lar and aperiodic voices. Methodological issues regarding jitter and shimmer have received considerable attention. Jitter and shim- mer have been found to be sensitive to variations in microphone type and placement, 56 recorder and tape types, 57,58 sampling size or signal length, 59 noise, 60 extraction algorithm, 61 and analysis systems. 62,63 Figure 4A and Bdemonstrates that cor- relation dimension is more robust to the effects of shorter signal lengths and lower sampling rates than jitter and shimmer calculated with MDVP. 55 Figure 4A shows the effect of signal length on the mean values of jitter, shimmer, and correlation dimension analysis of 14 nearly periodic voices. With MDVP, shimmer gives stable results when signal lengths are higher than 200 ms (48.6 cycles), which is the minimum signal length required for MDVP analysis, and jitter gives stable results when signal lengths are higher than 500 ms (about 122 cycles). In compari- son, correlation dimension analysis is stable when signal lengths are higher than 20 ms (about 4.8 cycles). Figure 4B illustrates the effect of sampling Journal of Voice, Vol. 20, No. 1, 2006 FIGURE 3. The time variances of jitter, shimmer, and correla- tion dimension for 11 voice segments selected from the type 3 voice in Figure 1 using a running window with length 400 ms, where curves I, II, III, IV, V, and VI correspond to D 2 of the periodic voice, D 2 of the aperiodic voice, jitter of the periodic voice, jitter of the aperiodic voice, shimmer of the periodic voice, and shimmer of the aperiodic voice, respectively. rate on the mean values of jitter, shimmer, and corre- lation dimension analysis. Jitter and shimmer both give stable results when the sampling rate is above 25 kHz, which is the minimum sampling rate required for MDVP analysis. Correlation dimension yields stable estimates even when the sampling rate is decreased to 2 kHz. Sampling noise resulting from low sampling rates may disrupt pitch tracking and estimation of jitter and shimmer. Correlation dimen- sion does not require measurement of cycle period and so does not share this limitation of jitter and shimmer. Correlation dimension avoids some methodological issues associated with perturbation methods. Additionally, applying the correlation di- mension might reduce experimental costs because lower quality recording equipment could be used by researchers. Nonlinear dynamic analysis may be valuable for describing irregular laryngeal activities, exploring new methods for diagnosing laryngeal pa- thologies, and assessing the effects of treatment of laryngeal pathologies. More support for these claims will be furnished in the following sections on vocal fold models, excised larynx experiments, and human voices analysis. VOCAL FOLD MODELS Motivations for designing computer models of the vocal folds have ranged fromspeech synthesis to CHAOS IN VOICE 7 FIGURE 4. The effects of signal length and sampling rate on estimation of jitter, shimmer, and correlation dimension. A. Signal length. B. Sampling rate. medical applications. Because vocal fold models give researchers complete control over phonation parameters, which allows simulation of a wide range of phonation conditions, they have been important to the study of irregularities associated with laryngeal pathologies such as vocal fold paralysis 12,17,64,65 and vocal nodules and polyps. 16,66,67 Many simplied versions of the IshizakaFlanagan 68 vocal fold model have been proposed for study, in which sev- eral mass, damping, and stiffness parameters are applied to model vocal fold vibrations. However, the exact relationship of the mass and stiffness of these lump parameter models with the biomechani- cal properties of vocal fold tissue is unclear. Finite element models, on the other hand, allow us to con- sider the biomechanical properties of vocal fold Journal of Voice, Vol. 20, No. 1, 2006 tissue, but they lead to large numerical calculations that complicate analysis. 67,69 Models can simulate irregular vocal fold vibra- tions. Chaotic vibrations may occur when aero- dynamic and biomechanical parameters, such as subglottal pressure, stiffness, mass, and tension, are out of the range that produces regular vibrations. 11,14 Figure 5A shows the effect of subglottal pressure on vocal fold vibrations in a symmetric two-mass model, where the maximal amplitude of the right lower mass x 1 was obtained with a Poincare map at a zero velocity plane 1 0. In a Poincare map, dynamical systems are illustrated as follows: A simple periodic orbit appears as a single point, a periodic orbit with nite commensurable frequency components gives rise to several discrete points, andchaoticbehavior is shownas scatteredpoints with a fractal structure. We use the default values of mass, stiff, and damping, and we provide all parameters in units of centimeters, grams, and milliseconds and their corresponding combinations. 14 Signicantly, small subglottal pressures fail to drive vocal fold vibrations. If subglottal pressure exceeds the phona- tion threshold pressure, periodic vocal fold vi- brations result. However, if subglottal pressure is excessively increased, nonlinear effects in the vocal fold system become important and vibrations are irregular and chaotic. Turbulent noise and random parameter perturbations, which might result from neurological and biomechanical effects, may broaden the range of parameter values that produce aperiodic vibrations. 15 Asymmetry between the vocal folds may also induce chaos. In an asymmetric model, one vocal fold has normal values for biomechanical parameters such as mass, stiffness, and tension, whereas the other side has abnormal values. The early study by Isshiki et al 64 showed that tension imbalances between the vocal folds produced subharmonics. With a simplied version of the IshizakaFlanagan model, 68 Steinecke and Herzel 12 found that when tension parameter Q deviates from 1, chaotic vibra- tions might occur that are relevant to disordered voices from patients with superior and recurrent nerve paralysis. Asymmetric stiffness and mass also may induce subharmonics and chaotic vibrations. Figure 5B shows the dependence of the maximal amplitude of the right lower vocal mass x 1r 12 on JACK J. JIANG ET AL 8 FIGURE 5. A. Effect of subglottal pressure on vocal fold vibrations in a symmetric two mass model, where the maximal amplitude of the right lower vocal mass x 1 was obtained using a Poincare map at 1 0. B. The dependence of the maximal amplitude of the right lower vocal mass x 1r on the uniform asymmetric stiffness parameter K un . the uniform asymmetric stiffness parameter K un , where the subglottal pressure is 0.012-cm H 2 O. K un 1 corresponds to symmetric stiffness, and K un 1 corresponds to asymmetric stiffness. When the difference between the stiffness of the vocal folds is signicantly large, subharmonics result. Asym- metric vocal fold stiffness is found in patients with vocal fold scar and Parkinsons disease. Subhar- monic patterns also have been found in multiple mass models with uniform and local asymmetries in vocal fold mass and stiffness. 65 Signicant changes in the mechanical structure of the vocal folds, such as through the introduction of mass lesions, like vocal polyps, nodules, cysts, or the Reinke edema, may cause the vocal folds to Journal of Voice, Vol. 20, No. 1, 2006 vibrate chaotically during phonation. The vocal fold model with a unilateral vocal polyp developed by Zhang and Jiang 16 shows that vocal polyps interfere with glottal closure and cause nonzero direct current (DC) ow (Figure 6A). Increasing vocal polyp size increases vocal-fold asymmetry and strengthens the nonlinear interactions of the vocal polyp and the vocal folds, which produces a greater perturbation of vocal fold vibrations. Figure 6B shows the effects of polyp size S 0 on the maximal amplitude of the left lower vocal mass x 1l in the vocal fold model, where S 0 is a dimensionless parameter of polyp size, 16 and polyp length, depth, and height are uni- formly changed. When the polyp size S 0 /1, which corresponds to a very small polyp, the periodic state of the vocal fold vibrations does not qualitatively change. However, when S 0 is sufciently increased, chaotic vibrations appear. This result suggests that an increase in polyp size would produce a decline in voice quality. Conversely, a signicant reduction in polyp size, such as would result from surgical excision, might reproduce periodic vibrations. Sur- gical removal of mass lesions has been clinically shown to lead to voice improvements, 7072 such as reduction of DC leakage and perceptual rough- ness. The model with a vocal polyp may provide a theoretical approach to study the effects of clinical treatment of laryngeal mass lesions. Unlike lump parameter models, which treat the vocal fold as a system of masses and springs, nite element models take into consideration the biomechanical properties of vocal fold tissue. Find- ings from studies conducted with both types of models indicate that regular and irregular vocal fold dynamics are governed by nite degrees of freedom, which implies that low-order models are appropriate for studying irregular and regular vocal fold dynam- ics. In the elastic continuum model of Berry et al, 9 which possesses hundreds of degrees of freedom, two or three empirical eigenfunctions capture the main vibratory patterns of the vocal folds. These ndings are consistent with those of Neubauer et al, 73 who decomposed glottal contour patterns obtained from high-speed image sequences into vibratory modes. Neubauer et al 73 found that two eigenfunctions captured approximately 98% of the glottal dynamics for normal phonations and that a minimum of three eigenfunctions were needed to CHAOS IN VOICE 9 FIGURE 6. A. Glottal volume velocity ow U for the normal vocal folds and vocal folds with a polyp. B. Effect of vocal polyp size S 0 on the maximal amplitude of the left lower vocal mass x 1l in the vocal fold model. capture the vibration patterns associated with bi- phonation (the existence of independent vibratory frequencies). Nonlinearity is a fundamental aspect of the laryn- geal system. If the laryngeal systems were linear, chaotic vibrations would not result when biome- chanical parameters like tension and subglottal pres- sure exceed the range of normal values, nor would they occur when parametric asymmetries exist be- tween the vocal folds, or when vocal fold morphol- ogy is altered by the presence of a vocal mass. Bifurcation and chaos are frequently observed in voices from patients with laryngeal pathologies. Nonlinear vocal fold models can test the application of nonlinear dynamic methods to study irregular vocal fold activities as well as to simulate pathologi- cal conditions and the effects of clinical treatment. Journal of Voice, Vol. 20, No. 1, 2006 Disordered voices from patients with laryngeal pa- thologies may have a nite yet higher dimension than voices from normal subjects, which indicates more complex dynamics, and successful clinical treatment of disordered voices may result in a lowered dimen- sion. This result has recently been examined through nonlinear dynamic analyses of excised larynx phonations and human voices. EXCISED LARYNX EXPERIMENTS Excised larynx experiments offer two main advan- tages over model studies: (1) an excised larynx more closely resembles the morphology of the in vivo larynx than a computer model, and (2) excised larynx experiments permit direct observation of vocal fold vibrations. Otherwise, excised larynx experiments offer many of the same advantages that models offer over human voice analysis: The phonation parame- ters in excised laryngeal experiments can be system- atically monitored and independently controlled to meet specic requirements, which include extremes that are difcult to obtain in humans; conditions may either be kept constant or changed gradually to study bifurcations from one vibratory regime to an- other; stationarity and signal length are easy to control because the parameters controlling phon- ations, eg, subglottal pressure, can be sustained for long periods of time; and nally, direct measurement of important data is easy and there is no need to bother with human subjects. As a result of these advantages, excised larynx experiments have been applied from a very early date to understand phona- tion and have recently studied irregular laryngeal behavior. 74 Van den Berg and Tan 75 reported that at high subglottal pressures, the glottis acquired an irregular curve and noise dominated the voice signal. Isshiki et al 64 studied asymmetrical tension in excised laryn- ges and a computer model, and they found that tension imbalances induced complicated and irregu- lar vibrations. With bifurcation analysis, Berry et al 18 observed that voice instabilities resulted from changes in subglottal pressure and vocal fold asymmetries. Svec et al 19 studied chest-falsetto reg- ister jumps in human subjects and excised human larynges. They found that a small change in vocal- fold tension might cause an abrupt change in register JACK J. JIANG ET AL 10 and pitch. Jiang and Titze 76 dened and measured the phonation instability pressure (PIP) to determine the irregular phonation (IP) range. Vocal fold vibra- tions became irregular and phonation perceptually rough when subglottal pressure exceeded the PIP. Our recent study suggests that these irregular vibrations may be chaotic. 20 We used an excised larynx setup to study excised larynx phonations while varying subglottal pressure and to compare nonlinear dynamic analysis with perturbation analysis. The larynges were mounted on an apparatus described in detail by Jiang et al 20 The acoustic signal picked up by the microphone was audio-to-digital converted at the sampling frequency 20 kHz and processed on a computer. We selected the middle segments of phonation samples with a length of 2 s for analysis. Traditional voice analysis methods, including voice spectrograms, jitter, and shimmer, were calculated. The software Cspeech 4.0 (Kay Elemetrics Corporation) extracted the measures of percent jitter and percent shimmer. Excised larynx phonations were studied while in- creasing subglottal pressure. The subglottal pressure P s 8-cm H 2 O drove normal and periodic vocal fold vibrations. A range of subglottal pressures ex- isted in which vibrations sustained a nearly regular and periodic pattern. However, when P s exceeded this range, irregular vibrations were produced and sound became rough. The minimum value of P s needed to produce voice instabilities has been de- ned as the PIP. 76 When subglottal pressure was increased above the PIP, irregular vibrations resulted andwererecordedforanalysis. WhenP s increasedfrom 8-cm H 2 O to 12-cm H 2 O and from 8-cm H 2 O to 16- cm H 2 O, the vibratory patterns of the excised larynx showed a period-doubling bifurcation and a quick transition from periodic motion to chaos, respectively, as shown in Figure 7A and B, respectively. 20 The phenomena of the period-doubling bifurcation and the quick transition from periodic motion to chaos can also be observed in a hemi-larynx, as illustrated in Figure 7C, and D, respectively. Chaotic vibrations may occur in excised larynx experiments when sub- glottal pressure exceeds the normal phonation range. A similar phenomenon, called above range phona- tion, was found in a symmetric computer model. 14 Quick transitions from periodic motion to chaos as well as from period-doubling bifurcation to Journal of Voice, Vol. 20, No. 1, 2006 chaos are found both in excised larynx experiments and in theoretical models, 11,14,18,20 which demon- strate that experimental observations in excised la- rynges have qualitative similarities with computer simulations of vocal fold vibrations. Figure 8A and B show the time series and fre- quency spectrum of a normal excised larynx phona- tion, respectively, and Figure 9Aand Bshowthe time series and frequency spectrumof an irregular excised larynx phonation, respectively. 20 The normal phona- tion (NP) has a periodic time series and discrete frequency peaks. In contrast, the IP has an aperiodic time series and a noise-like broadband frequency spectrum. Correlation dimension D 2 and maximal Lyapunov exponent 1 of the NP were estimated as D 2 1.05 0.02 and 1 0 bits/T s . D 2 and 1 of the IP were estimated as D 2 2.68 0.03 and 1 0.039 bits/T s . The periodic time series, discrete frequency peaks, correlation dimension D 2 1.05, and maximal Lyapunov exponent 1 0 show that the NP has regular characteristics. On the other hand, the aperiodic waveform, broadband frequency spectrum, correlation dimension D 2 2.68, and posi- tive maximal Lyapunov exponent 1 0.039 indicate that the IP has chaotic dynamics. Figure 10 shows the distributions of two nonlinear dynamic measures (correlation dimension D 2 and maximal Lyapunov exponent 1 ) and two perturba- tion measures (jitter and shimmer) calculated for 20 irregular excised larynx phonations (IP) and 20 normal excised larynx phonations (NP), which corre- spond fromleft to right to jitter, shimmer, correlation dimension D 2 , and maximal Lyapunov exponent 1 , respectively. 20 t tests were performed on these four measures. The differences between the IPs and NPs for jitter (t 2.35, P 0.01) andshimmer (t 1.58, P 0.1) are not signicant at the .01 level. In con- trast, D 2 s(t 5.48, P 0.0001) and 1 s(t 8.67, P 0.0001) of the IPs and NPs are signicantly dif- ferent at the 0.01 level. These results suggest that jitter and shimmer should be applied with caution, particularly when aperiodic or chaotic voice signals are being analyzed; however, nonlinear dynamic methods may provide valuable analysis tools. NONLINEAR TIME SERIES ANALYSIS OF DISORDERED VOICES Clinical observations demonstrate that most la- ryngeal diseases cause changes in voice quality, CHAOS IN VOICE 11 FIGURE 7. A. Period-doubling bifurcation exhibited by the excised larynx. B. Quick transition from periodic motion to chaos exhibited by the excised larynx. C. Period-doubling bifurcation exhibited by the hemilarynx. D. Quick transition from periodic motion to chaos exhibited by the hemilarynx. which results in voice irregularities and voice insta- bilities. Laryngeal stroboscopy and high-speed pho- tography have revealed that pathologies can lead to irregular vibratory patterns of the vocal folds. 13,73 Nonlinear dynamic methods are capable of analyz- ing irregular behaviors and might be valuable in several areas of voice study, including evaluation of clinical treatments, classication of voices according to the taxonomy of disorder proposed by Titze, 30 differentiation of normal and pathologic voices, and possibly diagnosis of laryngeal pathologies. Prelimi- nary studies have shown promise in these areas. Nonlinear dynamic methods have been applied to differentiate normal and pathological voices from patients with vocal polyps. 39 This study included voice samples from 68 patients with vocal polyps and 79 normal subjects. Subjects were asked to sustain the vowel /a/ at a comfortable pitch and intensity, as steadily and as long as possible. Figure 11 Journal of Voice, Vol. 20, No. 1, 2006 illustrates the correlation dimension D 2 distribution of all subjects. 39 Unlike random noise, the estimated D 2 of the samples from both the pathologic and the normal subjects are nite. The mean and standard deviation (mean 1.38, SD 0.24) of the D 2 of normal subjects voice samples are signicantly lower (t tests show P 0.001) than those of patho- logic subjects (mean 1.59, SD 0.34). This result suggested that the correlation dimensions of normal voices might be signicantly different from the correlation dimensions of voices from patients with vocal polyps. Titze et al 24 found that the corre- lation dimension of a dysphonic subject with polypo- sis was higher than that of a healthy subject. With the time series of fundamental frequency and ampli- tude peaks derived from microphone signals, Kakita and Okamoto 35 found that the median correlation dimension value of 17 dysphonic subjects was higher than that of 8 healthy subjects, which indicates that JACK J. JIANG ET AL 12 FIGURE 8. Normal excised larynx phonation. A. The time series. B. The frequency spectrum. perceptually rough voices have more complex dy- namics than normal voices. Hertrich et al 36 found that the electroglottographic signals of patients with Parkinsons disease and cerebellar diseases had signicantly higher fractal dimensions than the electroglottographic signals of normal subjects. Giovanni et al 37 used the maximal Lyapunov expo- nent to successfully differentiate between normal subjects and patients with unilateral laryngeal pa- ralysis. These studies show that both normal and pathologic voices may be low dimensional, and that nonlinear dynamic methods may describe the inuence of laryngeal pathologies on voice quality by differentiating pathological voices from normal voices. Nonlinear dynamic analysis is useful for classify- ing voice signals and represents a new approach Journal of Voice, Vol. 20, No. 1, 2006 FIGURE 9. Irregular excised larynx phonation. A. The time series. B. The frequency spectrum. that can supplement traditional analysis methods. Recently, nonlinear dynamic methods have been ap- plied to quantitatively study signal typing. 34 A total of 122 pathological sustained vowels from patients with Parkinsons disease, vocal nodules and polyps, laryngeal paralysis, and laryngeal carcinoma were evaluated. Figure 12A illustrates the estimated D 2 of the typical three types of signals in Figure 1, 34 where the curves I, II, III, and IVcorrespond to white noise, type 3, type 2, and type 1 signals, respectively. In contrast with the innite dimension of white noise, the estimated D 2 s of the type 1, 2, and 3 signals converge to 1.48 0.02, 2.16 0.04, and 3.56 0.04, respectively, with the increase of m. Cor- relation dimension tends to increase from type 1 to type 2 signals, and then again from type 2 to type CHAOS IN VOICE 13 FIGURE 10. Comparison of the distributions of jitter, shimmer, correlation dimension, and the maximal Lyapunov exponent for normal and irregular excised larynx phonations, where NP and IP correspond to normal and irregular phonations, respectively. The line inside the box marks the median, whiskers mark the 10th and 90th percentiles, and the dots mark the outlying points. 3 signals. For all 122 voice samples, the D 2 distribu- tions of the three types of signals are shown in Figure 12B. 34 We used a KruskaiWallis one-way analysis of variance (ANOVA) on ranks on the D 2 values. Post hoc pair comparison tests with the StudentNewmanKeuls method revealed a statisti- cally signicant difference between any two types of signals (P 0.001). D 2 s of the nearly periodic type 1 signals are statistically lowest. D 2 s of the type 2 signals, which contain periodic modulations and bifurcations, are statistically higher. D 2 s of the aperiodic type 3 signals are statistically highest. Thus, correlation dimension analysis effectively classies the three types of signals. Perturbation analysis has been applied to objec- tively evaluate the effects of surgical treatment of laryngeal pathologies. 43,70,72 However, as discussed here, perturbation analysis is only reliable for nearly periodic voice signals under limited conditions. Nonlinear dynamic methods can complement pertur- bation analysis methods because they can effectively analyze aperiodic voices, and they may be useful for assessingtheeffects of laryngeal surgeryandother Journal of Voice, Vol. 20, No. 1, 2006 voice treatments. This hypothesis is supported by our study of voices before and after surgical excision of vocal polyps, in which we used two nonlinear dynamic measures (correlation dimension D 2 and second-order entropy K 2 ) and two perturbation measures (jitter and shimmer) to assess the effects of surgical excision of polyps. 41 Jitter and shimmer were estimated with MDVP. Nineteen patients with vocal polyps (13 women and 6 men) were included. The average age of the patients was 41.6 years old (standard deviation 7.4). Patients received evaluation before and after surgical excision of polyps. For all nearly periodic voice samples re- corded before and after surgery, Figure 13 shows the distributions of jitter, shimmer, D 2 , and K 2 for the presurgery and postsurgery groups, respectively. 41 The results of a MannWhitney rank sum test showed that although jitter decreased signicantly after surgery (P 0.001), shimmer was not signi- cantly different for the presurgery and postsurgery groups at the .05 signicant condence level. On the other hand, for both nearly periodic and aperiodic voices, the correlation dimension and second-order JACK J. JIANG ET AL 14 FIGURE 11. Correlation dimension distributions for the normal and vocal polyp groups. entropy showed a statistically signicant decrease (P 0.001) after vocal polyp excision. Correlation dimension and second-order entropy analysis dem- onstrated that both presurgical and postsurgical voices were low dimensional and that postsurgical voices had decreased dynamical complexity and in- creased dynamical predictability. These ndings are in agreement with the ndings of the study of a vocal fold model with a unilateral vocal polyp, 16 which is discussed in the section on vocal fold models. Although nonlinear dynamic analysis methods are potentially valuable tools for studying voice, practi- cal issues exist in the application of these analysis methods, particularly issues resulting from the ef- fects of noise and the complexity of numerical algo- rithms. Development of simple and robust methods for analyzing chaotic activities in voice is important for routine clinical applications. More studies are needed to resolve these issues and improve the appli- cability of nonlinear dynamic analysis methods to voice study. CONCLUSIONS In this article, we reviewed some recent work in the application of chaos theory and nonlinear dynamic analysis methods to the study of com- puter models of the vocal folds, excised larynx experiments, and human voices. The combined application of computer model studies, excised Journal of Voice, Vol. 20, No. 1, 2006 FIGURE 12. A. Estimated correlation dimensions of the typi- cal three types of signals in Figure1, as well as white noise, where the curves I, II, III, and IV correspond to white noise, type 3, type 2, and type 1 signals, respectively. B. The distributions of correlation dimensions for the three types of voice signals. larynx experiments, and analyses of human voice data can greatly enhance our understanding of chaos in voice production and its relationship to voice instabilities and disorders. Preliminary applications of chaos theory and nonlinear dynamic methods to the study of voice hold great promise. More studies are needed to examine the clinical relevance of these newconceptual and analytic tools. Practical analysis methods need to be developed and tested, and more extensive evaluations, larger numbers of subjects, and more types of laryngeal pathologies are needed to examine the applicability of nonlinear dynamic analysis. Perturbation analysis of voices became popular in the last decades although the limitations of such methods have been widely accepted. Nonlinear dy- namic methods complement traditional analysis CHAOS IN VOICE 15 FIGURE 13. The distributions of jitter, shimmer, correlation dimension, and second-order entropy before and after surgery, where A and B correspond to after and before surgery, respectively. The line inside the box marks the median, whiskers mark the 10th and 90th percentiles, and the dots mark the outlying points. methods. Nonlinear dynamic analysis methods need not replace existing methods, but they could improve the array of voice analysis tools available to the clini- cian. 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