Discharge Characteristics of Laryngeal Single Motor Units During Phonation in Young and Older Adults and in Persons With Parkinson Disease

Erich S. Luschei,1 Lorraine O. Ramig,2,3 Kristin L. Baker,3 and Marshall E. Smith4

 1Department of Speech Pathology and Audiology, University of Iowa, Iowa City, Iowa 52242;  2Department of Speech, Language, Hearing Science, University of Colorado, Boulder, Colorado 80309;  3Wilbur James Gould Voice Research Center, Denver Center for Performing Arts, Denver, Colorado 80204; and  4Division of Otolaryngology, University of Utah School of Medicine, Salt Lake City, Utah 84132


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Luschei, Erich S., Lorraine O. Ramig, Kristin L. Baker, and Marshall E. Smith. Discharge characteristics of laryngeal single motor units during phonation in young and older adults, and in persons with Parkinson disease. The rate and variability of the firing of single motor units in the laryngeal muscles of young and older nondisordered humans and people with idiopathic Parkinson disease (IPD) were determined during steady phonation and other laryngeal behaviors. Typical firing rates during phonation were ~24 s/s. The highest rate observed, during a cough, was 50 s/s. Decreases in the rate and increases in the variability of motor unit firing were observed in the thyroarytenoid muscle of older and IPD male subjects but not female subjects. These gender-specific age-related changes may relate to differential effects of aging on the male and female voice characteristics. The range and typical firing rates of laryngeal motor units were similar to those reported for other human skeletal muscles, so we conclude that human laryngeal muscles are probably no faster, in terms of their contraction speed, than other human skeletal muscles. Interspike interval (ISI) variability during steady phonation was quite low, however, with average CV of ~10%, with a range of 5 to 30%. These values appear to be lower than typical values of the CV of firing reported in three studies of limb muscles of humans. We suggest therefore that low ISI variability is a special although not unique property of laryngeal muscles compared with other muscles of the body. This conceivably could be the result of less synaptic "noise" in the laryngeal motoneurons, perhaps as a result of suppression of local reflex inputs to these motoneurons during phonation.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Although there is currently a great deal of information about the firing characteristics of motor units in limb and hand muscles of the human body (see Table 3), there is little information about the behavior of human laryngeal motor units (LMUs). Chanaud and Ludlow (1992) reported on LMU behavior related to quiet respiration, Faaborg-Andersen (1957) illustrated a few records of LMUs during phonation, and Larson and colleagues (1987) demonstrated small brief changes in the fundamental frequency of vocal fold vibration (Fo) that immediately followed the discharges of LMUs. There has not been however a systematic study of firing rates and interspike interval (ISI) variability of LMUs during steady-state phonation. This information could allow a comparison with similar measurements that were made on other human muscles. Typical firing rates would provide suggestive evidence about the contraction speed of the human laryngeal muscles, which has been thought to be "fast" on the basis of direct measures in cats (Hirose et al. 1969) and dogs (Hast 1966; Mårtensson and Skoglund 1964). There have been no in vivo direct measures of the contraction time of human laryngeal muscles (with a force transducer attached directly to the stimulated muscle). The techniques necessary to stabilize the position of the larynx and isolate the pull of the stimulated muscles cannot be used in a human. Thus less direct methods must be used to estimate the speed of contraction of human laryngeal muscles. Kempster and colleagues (1988) measured the time course of changes in Fo after electrical stimulation of laryngeal muscles of humans who were phonating at a steady Fo. These authors suggested a contraction time of ~35 ms in the human, which is twice as long as the contraction time reported in the thyroarytenoid (TA) muscle of the dog and cat. It should be noted however that the indirect method used by Kempster et al. may be affected by factors that are not represented in the methods used with animals, e.g., the nonisometric condition of the contracting muscle in the human. Knowledge of typical firing rates in human laryngeal muscles could help clarify whether there is a species difference in this characteristic of laryngeal muscles. If, for example, human laryngeal and limb muscles fire spontaneously at similar rates during normal activity, then one could infer that these muscles have similar contraction speed. The ISI variability could potentially be related, in current models (Matthews 1996), to the mechanisms of repetitive firing and synaptic noise in laryngeal motoneurons.

There are characteristic changes in the voice of both elderly people (Liss et al. 1990; Murty et al. 1991; Ramig and Ringel 1983; Wilcox and Horii 1980) and people who have idiopathic Parkinson Disease (IPD) (Dromey et al. 1995; Gamboa et al. 1997; Gentil et al. 1995; Perez et al. 1996). The changes in the larynx and its control system that are the primary causes of the "old voice" and the weak and breathy voice of the person with IPD are not established, however. These voice changes with age and disease could conceivably be related in part to changes in the rate and variability of the firing of laryngeal motoneurons. It was reported that the rate of motor unit firing in limb muscles is decreased and the ISI variability is increased in elderly individuals (Nelson et al. 1984; Soderberg et al. 1991). Dengler and colleagues (1986) observed an increase in variability but not a change of firing rate of single motor units in the first dorsal interosseus muscle in individuals with IPD compared with healthy control subjects. Titze (1991) has shown, in a biomechanical model of voice production, that the rate and variability of the firing of laryngeal motoneurons could have large influences on the stability of Fo, which would therefore influence the stability of the perceived pitch of the voice. In addition, Rossi and colleagues (1996) presented evidence for decreased fatigability and hypertrophy of type 1 muscle fibers in tibialis anterior of people with Parkinson disease.

Summarizing, we addressed two primary questions in this study. First, are the rate and ISI variability of LMUs during steady phonation similar to these firing characteristics of motor units of other human skeletal muscles during steady contraction? Second, do the firing characteristics of LMUs change with age and/or with IPD?


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The data analyzed for this report come from a more general study of laryngeal muscle behavior in young and elderly nondisordered subjects and people with IPD. Although the electromyographic (EMG) electrodes used in this general investigation were designed to record wide-field EMG signals to provide a quantitative estimate of the degree of muscle activation during a variety of speech and phonation behaviors, they also provided, in many subjects, very usable records of single motor unit activity. Such records were adequate, with careful marking, to determine the rate and variability of LMU firing during steady phonation.

Subjects

Recordings that contained isolated single motor units responses were obtained from 31 subjects. These subjects were grouped into three categories, depending on age and disease status. Characteristics of the ages are shown in Table 1. The "young" and "older" subjects were all healthy, free of any neurological disease, and had normal voices for their age. The "older" group was composed of those nondisordered subjects who were 60 yr of age or older and had the characteristics of an "aged" voice, i.e., hoarseness, reduced loudness, unsteadiness, and evidence of mild glottal incompetence. This determination was based on audio perceptual and videoendoscopic screening. The IPD subjects were all diagnosed with IPD and were under the care of a neurologist. All were taking anti-Parkinson's drugs and were using their medications in their typical manner at the time of the recordings. Although these IPD subjects were "mild" to "moderate" in the general symptoms of IPD, they were selected based on audio perceptual and videoendoscopic screening to have classic characteristics of voice in IPD, e.g., weak breathy voices and mild to moderate glottal incompetence (vocal fold "bowing").


                              
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Table 1. Gender and age of subjects in the young, older, and IPD groups

There were two IPD subjects less than 60-yr-old, one 50 and the other 58. It should be noted, however, that there were no LMUs recorded from the 50-yr-old IPD subject that could be used for the quantitative analysis presented in the RESULTS (STEADY PHONATION GROUP). Therefore there is no overlap in the age ranges of the young and IPD groups in terms of the quantitatively based conclusions of this report. On the other hand, the ages of the older and IPD groups are very similar. Therefore, changes observed in the IPD group may also reflect changes associated with the aging process.

The experimental protocol was approved by the Human Subjects Research Committee of the University of Colorado-Boulder.

Overview of the intrinsic muscles of the larynx

The intrinsic laryngeal muscles studied in this report were the TA, the cricothyroid (CT), and the lateral cricoarytenoid (LCA). The TA and LCA are laryngeal adductors. They close the glottis tightly during swallowing, coughing, and for maneuvers such as the valsalva. They are also active during speech; they bring the vocal folds to a closed position, which allows the air stream to cause vocal fold oscillation. The CT is considered a laryngeal adductor, although it primarily elongates the vocal fold. It is particularly important in raising the frequency of vocal fold oscillation and becomes very active during the production of high-pitch phonation. For more detail on the laryngeal muscular actions and aerodynamics of vocal fold vibration, see Titze (1994).

Electrode placement

The electrodes used to record the laryngeal muscle activity were bipolar hooked-wire electrodes made from two strands (bifiler) of 0.002-in. diam insulated stainless steel wire. The bifiler wire was placed in the lumen of a 1.5-in. 25-gauge hypodermic needle. A flame was used to burn the insulation away for ~1.5 mm of each wire in the "hook." Hypodermic needles carrying the electrode wires were inserted through the CT membrane and directed laterally and rostrally in the submucosa to the TA muscle and laterally and slightly caudally to the LCA muscle. The belly of the CT was palpated through the skin of the neck, and electrodes were inserted into it, using care to make sure the electrodes did not enter the overlying strap muscles.

Electrode characterization procedures

The EMG activity from each electrode was observed during several behaviors to determine whether the electrode was in the intended muscle. For the TA and LCA, strong activity during swallow, valsalva, and high and loud phonation and absence of activity during rapid inspirations indicated a successful insertion. These two muscles behaved, in our experiments, in a highly parallel fashion. However, our designation of an "LCA" electrode was based on its simple adductor-like behavior and its being placed caudal to the TA electrode. There are no well-established EMG behavioral criteria for distinguishing LCA from TA. For the CT muscle, strong activation during high-pitch phonation, the suppression of background activity during low-pitch phonation, and the absence of EMG activity when the subject attempted to push the chin down against resistance indicated a successful CT insertion.

Recording procedures

Variable inductance plethysmograph bands were placed around the chest and abdomen of the subject to document relative changes in lung volume. The subject was seated in a dental chair, which was initially placed in a recumbent position to insert the electrodes. Data were collected, however, with the subject in a comfortable sitting position. A small head-mounted microphone (model C410, AKG Acoustics) was placed close to the mouth to record the voice. A sound level meter, placed 30 cm from the subject's mouth, was used to measure the sound pressure level of the voice. The EMG signals were amplified with optically isolated amplifiers (band-pass 30 Hz to 5kHz). All signals were anti-alias filtered at 2.5 kHz and then recorded on a DAT instrumentation recorder and/or digitized directly to computer disk. The A/D sample rate for both the DAT and the computer acquisition was 5 kHz/channel, which is somewhat low for optimal study of motor unit waveforms. We were, however, limited in our sampling rate because of our instrumentation. Although this sampling rate probably inflated the variability of the amplitude and duration measures of the LMU potentials, we do no think it had a significant effect on our measures of firing rate and ISI variability.

Characterization behaviors, such as swallowing, the valsalva maneuver, and phonating a high pitch were recorded at the beginning of the session and again at the end if the session if it had not been terminated by the loss of electrodes or at the subject's request. After the initial characterization behaviors, the subjects produced steady phonation at their self-selected normal pitch and loudness for as long as possible and subsequently at various combinations of loudness and pitch for ~2 s. Recordings were also made during reading of phrases, monolog (telling about the "happiest day of your life"), and rest breathing.

Data analysis

The entire record of each subject was inspected on a computer monitor by one of the authors (Luschei). Sections of the record where a motor unit in one of the muscles could be unambiguously identified were noted. After reviewing the entire record, separate computer files were made of a short section in each record where unit isolation was the best. Unit discharges in each file were marked by an analysis feature of the computer program, with a simple amplitude criterion set by the observer. The peaks of units above (positive-going peaks) or below (negative-going peaks) the amplitude criterion were detected and marked by a computer algorithm. Subsequently, each mark was checked by an observer against the actual unit waveform. Special attention was directed to unusually short or long intervals. In the vast majority of cases, these were due to the intrusion of another unit or a low-amplitude spike from the unit under study. Such marks were either deleted or added based on the unit waveform and with the assumption that the ISI of a tonically firing motor unit will not suddenly decrease to one-half or less or increase to double the preceding and following intervals. If, however, a suspected "extra" spike had the same waveform as the unit under study, the mark was not deleted. Similarly, if a suspected "missing" mark did not have an accompanying unit waveform that was reasonably close to the unit under study, a mark was not added.

The ISIs defined by these marks were transferred to a spreadsheet program, and a curve showing the ISIs as a function of time was created. The portion of this curve where the ISIs were not changing significantly over time and where the moving average of the ISI was lowest was selected (see Fig. 2) for calculation of the mean, SD, and CV of the period of steady firing. It should be noted that this definition of the period of "steady phonation" was based on the LMU's behavior. However, the Fo and gross EMG levels of the muscles being recorded were also steady during these periods. Of the units to be presented in RESULTS, the minimum number of ISIs for calculation of these statistics was 10, the maximum was 128, and the mean was 39.

The duration of the waveform of 10 motor unit potentials in each unit file was measured by an observer by marking the beginning and end of the waveform. We attempted to make these consecutive waveforms but skipped those that were disturbed by intrusion of smaller units. The peak-to-peak amplitude of the spike-like portion of each unit was estimated by measuring a waveform whose amplitude was approximately halfway between the maximum and minimum amplitude of other potentials from this unit during the record.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Qualitative aspects of recruitment and maximal firing rates

In most cases, there was little opportunity to study the recruitment of LMUs. We were able to obtain, however, several records of identifiable motor units during slow gradual increases in the frequency of phonation (voluntary "pitch ascensions"). Figure 1 illustrates such a record. A single motor unit, identifiable in the initial portion of the CT EMG, begins firing at a rate of ~6 s/s and then increases its rate even before phonation begins (~0.5 s later than the first unit discharge). The firing rate continues to increase as Fo increases, but unit firing rate becomes stable (arrow) at an ISI of ~42 ms, although the Fo continues to increase. After ~2.5 s into the record, the single motor unit waveform can no longer be separated from the EMG interference pattern, so one cannot determine whether this unit made further increases in its firing rate as the voice increased to its maximum Fo. From our few records of this type, it appears that LMUs are capable of exhibiting gradual systematic increases in firing rate during a task involving gradual increases in the activity of a muscle and that they can achieve steady firing rates of >20 s/s.



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Fig. 1. Top: electromyogram (EMG) of the cricothyroid (CT) muscle during a gradual increase to the highest pitch possible in a 55-yr-old male. Trace below the EMG is the vocal fold vibration (Fo); it changes from 100 Hz to ~600 Hz. The EMG trace is 11 s long and reaches a peak to peak amplitude of ~2.5 mV. Bottom: changes in the interspike interval (ISI) of the single motor unit identifiable during the first 2.5 s of the EMG record in association with the corresponding increase in the Fo. Arrow is discussed in text.

In two instances, we were able to observe a single motor unit during a cough. Figure 2 (right) illustrates such a case. Shortly after the data for the left hand side of Fig. 2 were recorded during sustained phonation, the subject coughed. Before any sound was produced by the cough, there was a brief episode of high-frequency firing in a motor unit from this same muscle. We presume that this occurred during a tight closure of the glottis during the buildup of the tracheal pressure. There was no sound produced during this period. This was followed by a series of cough sounds, each associated with one or two discharges from the motor unit. The minimum ISI during the period of high-frequency firing was 20 ms, and the first three couplets during the cough bursts were 31, 22, and 33 ms, respectively. Because the unit observed during the cough occurred shortly after the data of Fig. 2 (left) and because it had the same waveform, we think it is very likely that the units of Fig. 2 (right and left) were the same unit. There was an increase in the amplitude of the unit from 0.125 to 0.180 mV between these two records, but we observed amplitude changes of this magnitude when recording a continuous record of a single motor unit. One can conclude therefore that at least some LMUs can discharge at rates as high as 50 s/s. It should be noted, however, that we never observed ISIs, even for couplets, that were <20 ms, i.e., rates >50 s/s.



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Fig. 2. Left: CT single motor unit during steady comfortable phonation in a young female subject. The graph below shows the corresponding ISIs. Mean ISIs are discussed in text. Spike amplitude (top trace) was ~0.125 mV. Right: CT unit in this same subject during a cough. Trace below the unit record is the microphone signal. Record is 2.5 s long. ISI values are discussed in text.

Quantitative analysis of rate and variability

Quantitative determination of the rate and variability of LMU firing was based on relatively short periods of firing during steady phonation. A representative record is illustrated in Fig. 2, left. Because the first one-half of the record had shorter stable firing intervals, only the first 1.25 s of the record was used to calculate the mean and SD of the firing rates, which in this case were, respectively, 42.5 and 2.9 ms. Thus the CV was 7%. The voice was very steady during this interval; the CV of the Fo, which had a mean of 229 Hz, was only 0.6%.

A total of 122 units were identified that were of sufficient quality and record duration to characterize their pattern of firing. These were observed during a wide variety of behaviors. Most (n = 70) were observed during steady-state phonation, and it is this group of units that will be considered in detail (average and range of units/subject were 2.4 and 1-7, respectively). It should be realized, however, that this group encompasses a considerable variety of phonations. Approximately one-half were observed during "normal pitch and loudness" (n = 36), but the remainder were associated with loud, soft, or high pitch phonations. Although there is obviously different control of these muscles to produce this variety of voices, the ISIs did not differ significantly when the different phonation tasks were compared within the young, older, and IPD groups (P = 0.51, P = 0.84, and P = 0.41, respectively). Therefore units associated with these different types of steady phonation were simply classed as bring in the "steady phonation " group. The other 52 unit records, classed as the "other behavior" group, were obtained during speaking tasks, quiet resting respiration, the attempt on the part of the subject to perform a valsalva maneuver, or between periods of phonation when the subject was ready to speak. These latter units often fired regularly (definitely not showing a respiratory pattern), but because there was no phonation we do not feel that they can be included in the steady phonation group.

STEADY PHONATION GROUP. Figure 3, top bar graph, shows the means and SDs of the ISI's for the three groups of subjects. Units in each group were pooled across muscles. Because a statistical analysis (MANOVA) revealed a significant effect of gender (P = 0.01) for the mean ISI variable, males and females were analyzed separately. In all of the following statistical analyses the calculated P values were multiplied by the number of posthoc comparisons that were tested for each dependent variable (method of Bonferroni), and these adjusted P values were compared with P < 0.05 to test significance. There are three significant differences among the four comparisons made of the ISI values:



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Fig. 3. Comparison of the means and SDs of the ISI, CV, unit amplitude, and duration in the 3 groups of subjects. Top graph, solid bars: male subjects; open bars: female subjects. Males and females are combined in the lower 3 graphs because there was no gender effect for these variables. Numbers of units in each group are young males, 18; young females, 14; older males, 14; older females, 8; idiopathic Parkinson disease (IPD) males, 12; IPD females, 2. Statistical differences are presented in text.

Older male ISIs are greater than those of young males (P = 0.024).

IPD male ISIs are greater than those of young males (P = 0.04).

Older male ISIs are greater than those of older females (P = 0.04).

Because there were only two IPD female units, this group was not compared with any other; it was included in Fig. 3 only for completeness.

Before considering the CV of firing intervals of units in the steady phonation group, it is worthwhile to consider the shape of the distribution of intervals from individual units. The problem we face in this regard is that there were too few intervals for most of our units to create an interpretable histogram of firing intervals. There were, however, four units in the steady phonation group that had ~100 intervals or more. Their interval histograms are shown in Fig. 4. These distributions are all highly symmetric, with little suggestion of a rightward skew. If they are considered as representative of all units in the group, this symmetry would suggest that most units in the steady phonation group were firing at rates well above their minimal "just recruited" rate (Matthews 1996).



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Fig. 4. Frequency histograms of ISIs of 4 unit records. A: young subject; 2 histograms because there were 2 records available (n = 114 and n = 110). B: young subject; n = 128. C: older subject; n = 98. D: IPD subject; n = 128.

There was no gender effect on the CVs, unit amplitudes, or unit durations, so genders were combined for analysis of these three variables (Fig. 3). Although the CVs and unit amplitudes of the older and IPD groups were somewhat higher than the young group, there were no significant differences for these two variables. It may be noted, however, that the SD of the unit amplitudes of the older and IPD groups was greater than the SD for the young group. This was the result of some very large units in the former two groups. The largest unit in the young group was 0.88 mV. By comparison, there were three units in the older group that were larger than 0.88 mV, the largest being 1.4 mV, and two units in the IPD group larger than 0.88 mV, the largest being 1.9 mV. The mean duration of the LMU spikes was ~2.5 ms and did not differ among the three groups (Fig. 3, bottom bar graph).

Although units recorded from all three laryngeal muscles are represented in the steady phonation population, the vast majority of the units were recorded from either the TA (49%) or CT (33%). Considering that the contraction time of the TA muscle is shorter than the CT muscle in experimental animals (Hirose et al. 1969; Mårtensson and Skoglund 1964), it seemed worthwhile to compare the mean ISI during steady-state phonation between the TA and CT muscles. One would expect TA units to have lower mean ISIs than the CT if the TA muscle of the human has a shorter contraction time than the CT, i.e., is "faster," assuming the contraction time of a muscle is related to its typical spontaneous ISI. Looked at across all subject groups, there were no significant differences between these mean ISIs of the TA and CT. However, because there was a strong gender effect on the ISI values (Fig. 3, top bar graph), we also compared the TA and CT ISIs separately for males and females. Our comparison had to be restricted to the young and older groups, however, because there was only one CT unit from an IPD male. There was no significant difference between TA and CT for young and older females. The results were quite different for the males, however (Fig. 5, top bar graph). Six comparisons were made. There were two significant differences among these mean ISI values for the male subjects:
1. Older TA was greater than older CT (P = 0.030).
2. Older TA was greater than young TA (P = 0.003)



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Fig. 5. Comparison of the means and SDs of the ISI and CV of thyroarytenoid (TA) and CT motor units of males subjects. Solid bars: TA units; open bars: CT units. Only 1 unit was available for CT in the IPD males, so it was not plotted on the graphs. Statistical differences are presented in text. Number of units in each group: young TA = 6, young CT = 10, older TA = 7, older CT = 5, IPD TA = 9.

As noted earlier, there were no significance differences among the CV values when the young, older, and IPD groups were pooled across gender and muscles (Fig. 3, second from the top bar graph). Because we noted a difference in ISI values between TA and CT, however, we also tested CV values with CT and TA units separated (Fig. 5, bottom bar graph). Four comparisons were made. There was only one significant difference for these CV values:
1. Older TA was greater than older CT (P = 0.04).

The foregoing comparisons suggest that TA motor units fire more slowly with age, but only in males. Additionally, TA motor units are more variable than CT motor units in older males. There are, however, two facts that should be taken into account in generalizing this conclusion beyond the data used for the analysis. First, one would suppose that the nine IPD male TA units would also fire more slowly and variably if age was the primary factor (considering that the IPD males were approximately the same age as the older males). This was not the case however; the IPD male TA units had shorter ISIs than the older male TA units (although this difference did not reach significance). Second, the age effect on the ISIs seen in the older males in both Fig. 3 (top) and Fig. 5 (top) depends on seven motor units recorded from the TA in four subjects. Because there were only four older male subjects, these seven units represent most of the subjects in this group. However, four of these units were recorded from the same subject (#13), two units from the right TA, and two units from the left TA. One could be suspicious that these significant differences are being "driven" by data from one subject. Certainly these four units are influential, but if the four units recorded from subject 13 are eliminated, the remaining three older male TA units have mean ISIs that are longer than those of the young male TA units (67 compared with 43 ms). Thus there is some evidence that the age effect on ISIs is not solely dependent on one subject.

OTHER BEHAVIOR. Thus far, our analysis of firing rates of LMUs was during steady phonation. It could be reasonably argued that such rates are not necessarily representative of LMU activity during other activities of laryngeal muscles. To evaluate this possibility, we characterized the typical firing rates of units observed:
1. During quiet breathing (respiration).
2. When no phonation was present but the subject was prepared to phonate (no behavior).
3. During the valsalva maneuver (valsalva).
4. During periods of speaking.

Usually there was only a short period of firing to calculate the maximum rate of firing (except for valsalva maneuvers). During respiration, for example, we calculated the mean firing rates for the 10 intervals during the period of maximum activity. The means and SDs of the mean ISIs of the units included in the other behavior group are shown in Table 2. The number of units is not large, but the data suggest that the mean ISIs are in the same range of rates observed during steady phonation. During speech tasks, such as repetition of the phrase "Pop took his socks off," chosen because it involves repeated voicing and devoicing, the firing rate of LMUs changed over a large range but was patterned in a consistent way (Fig. 6). In these cases, the period of high-frequency discharges was too brief to calculate a mean rate. The minimum intervals were typically in the 40- to 50-ms range, however, suggesting the maximal rates during speech are also similar to rates observed in steady phonation.


                              
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Table 2. Mean ISIs and SDs of units recorded from young, older, and IPD subjects during other behaviors



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Fig. 6. Modulation of the firing of a CT single motor unit during 4 repetitions of the phrase "Pop took his socks off." Top trace: unit; its amplitude is ~0.250 mV. Middle trace: microphone signal. Bottom trace: large but patterned changes in the ISIs with speech. Minimal ISIs are ~40 ms.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Comparison of different groups of subjects

When the mean ISIs of units from older and IPD males were pooled across muscles, they were significantly longer than those of young males. If the ISIs from the male population were further fractionated into units recorded from the TA and CT muscles, there was evidence of an age effect on the mean ISI and CV of TA but not CT motor units. The ISIs of IPD male TA units were longer than those of young subjects, but this difference was not significant. Although there are cautionary factors to be considered when generalizing the results of our analysis, we feel the data are sufficient to suggest that the firing rate of TA motor units is decreased in older and IPD men. No such effect is seen in females or in the CT of either males or females. These results are similar in certain respects to two prior studies in which it was found that single motor units in the abductor digit minimi of older subjects had lower firing rates and more variability than units recorded in younger subjects (Nelson et al. 1984; Soderberg et al. 1991). Howard and colleagues (1988) also noted that motor units of the brachial biceps decreased their firing rate as a function of age. These authors did not find a gender effect, however. A study of single motor units firing in the first dorsal interosseus of Parkinson's disease subjects and matched controls during steady contractions of 10% of the maximal voluntary contraction found that mean firing rates were about the same (10/s) in the two groups but that units from the Parkinson's patients were twice as variable in their firing intervals as were those from control subjects (Dengler et al. 1986). Although ours and all of these earlier studies differ in the specifics of their results, they all support the general idea that motor unit rate and variability are affected in some degree by age and Parkinson's disease.

Our finding of age-related motor unit firing characteristics in men but not women appears to be unique compared with studies of motor units in limb muscles. It is noteworthy, however, that previous studies of age-related changes of the voice found clear gender differences. The Fo of the voice of men tends to increase with age, whereas it decreases in women (Higgins and Saxman 1991; Honjo and Isshiki 1980). Higgins and Saxman (1991) also noted that during vowel production in older men but not in older women there was greater glottal flow amplitude than there was in young men, a fact that might be related to decreased activation of the TA. Sapienza and Dutka (1996) observed no aging effect on phonation variables in their study of women. Thus we think that our observed gender effect, with men but not women showing the effects of age, may have functional correlates.

Comparing LMUs with motor units of skeletal muscles

Are laryngeal motor units in the human similar in most respects to motor units in human skeletal muscles, or do they have special properties? Given the short contraction times of laryngeal muscles of cats and dogs (Hirose et al. 1969; Mårtensson and Skoglund 1964), one might have expected that spontaneous motor unit firing rates of human laryngeal muscles would be substantially higher than those of human skeletal muscles. It appears, from our data, that this is not the case. We observed a range of firing rates of 5-6 to 50 s/s and a typical rate during phonation of ~24 s/s. These values are not obviously higher than the values reported in previous studies of motor unit firing rate and variability (Table 3). Therefore we suggest that human laryngeal muscles are probably no "faster" than other muscles of the body, although laryngeal muscles are clearly faster than limb muscles in cats and dogs. It should be noted that this conclusion makes the assumption that the contraction time of a muscle is directly related to the ISI of spontaneous firing during behavior. It should also be noted that the firing rates that appear in Table 3 represent in some cases our "best guess" in trying to provide a simple indication of the firing rates observed in these studies. These data are reported in a wide variety of ways. In some cases, we based our estimates on information provided in graphs and scatter plots. The description, in Table 3, of the behavior as "steady" refers to tasks where the directly measured force of contraction of the studied muscle was not changing over time, i.e., did not gradually increase or decrease.


                              
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Table 3. Reported firing rate (FR) and CV of single motor units in a variety of human muscles

One might wonder whether the motor units we reported are in the "just-recruited" portion of their range of firing rates and that the rates were therefore considerably lower than they would have been if the motoneurons were excited well beyond their recruitment threshold. We think this is unlikely for three reasons. First, we were able in a few instances (e.g., Fig. 1) to follow the firing rate of a motor unit during an ascending pitch phonation, where we observed a large increase beyond the rate at recruitment. Further the rate appeared to become stable, although the muscle as a whole continued to be recruited to higher levels of activity. The second reason is based on an earlier study (Hsiao et al. 1994), which reported on the firing rates of a very unusual CT single motor unit in the larynx of a trained singer. This unit could be clearly identified during all vocal behaviors, including a loud voice at the top of the singer's vocal range. During this "maximal phonation" behavior, the unit reached a firing rate of 30 s/s, only slightly higher than the rate of 24 s/s observed during phonations at normal pitch and loudness. The third reason is based on a model recently presented by Matthews (1996). Matthews argued that some features of the ISI distributions of motor units can be related to the time course of motoneuron afterhyperpolarization. In effect, the model suggests that, if a motor unit is just recruited and firing near the lower end of its range of firing rates, the ISI distributions for this unit will have a rightward-skewed "tail" (long intervals), whereas this tail would not be present if it were firing in the middle or upper portion of its range of rates. Thus the presence or absence of a tail on ISI distributions could potentially answer the question of whether our units were firing at or well above their minimal firing rates. Although we did not have sufficient data to compute ISI histograms for all our motor units, such a histogram could be computed for four units (Fig. 4). None of these four units exhibited a rightward scatter toward long intervals. Thus we think our rates reflect the activity of motoneurons driven well into the middle or upper regions of their range of firing rates. In making this suggestion, however, we also feel that LMUs may become excited to higher rates, at ~50 s/s, during "maximal" contractions such as those occurring during cough (Fig. 2).

The ISI variability of LMUs appears to be considerably lower than the variability of motor units of skeletal muscles (Table 3). Bigland-Richie and colleagues (1983) explicitly estimated the CV of the units they recorded during maximal contractions as being ~30%. It should be noted that their method of recording single motor units, by advancing a metal microelectrode through maximally contracting muscles, provided them with excellent (though brief) records of the potentials; the 30% CV was therefore not a product of extra nor missing spikes. Although the variability of firing of motor units in laryngeal muscles is low, the oculomotor system makes it clear that the laryngeal system is not unique in this regard. Fuchs and Luschei (1970) reported that the ISI CV of abducens motoneurons of the monkey during eye gaze fixation was ~10%. In addition, Matthews (1996) has shown that at least some low-threshold soleus motor units produce ISI CVs of ~10% when firing at their highest rates. Although the entire range of reported ISI CVs in the human should therefore be regarded as 10-30%, it is noteworthy that the modal ISI CV in our population of motor units was ~10%, and 43% of the motor units studied had CVs of <10%. Thus we would suggest the laryngeal muscles are "special" with regard to low ISI variability, although not unique in this regard among the motor systems of the body.

In Matthews model (1996), ISI variability is viewed as the effect of summing synaptic "noise" with the afterhyperpolarization of the motoneuron membrane voltage after an action potential. One source of such synaptic noise would be the result of small but continuous input from local reflex interneurons. It is possible that laryngeal motoneurons are subject to less synaptic noise during phonation compared with spinal motoneurons during steady contractions. This seems plausible. Laryngeal muscles have muscle spindles, but they are few in number (Larson et al. 1974; Rossi and Cortesina 1965), and there does not appear to be a stretch reflex (Testerman 1970) in this system. Of course, there are powerful reflex effects exerted on the laryngeal muscles by mechanoreceptors and chemoreceptors in the laryngeal mucosa and adjoining tissues (Davis et al. 1993), which are responsible for coughing and rapid glottal closure. Given the sensitivity of these afferents (Davis and Nail 1987) and their reflex connections it is difficult to explain why these reflexes do not normally interfere with phonation. Phonation produces vibration of all the tissues in the vicinity of the larynx, as anyone may ascertain by feeling the thyroid cartilage with the tip of their finger during phonation. To explain the lack of reflexes during phonation, it was suggested, as one possibility (Davis et al. 1993), that descending inputs to the laryngeal motor system suppress the reflex response to what is in fact a large afferent inflow from the laryngeal tissues. Were these afferent signals to produce synaptic effects on the laryngeal motoneurons during phonation, one would expect their ISI variability to be very high. In fact, it appears to be among the lowest reported for the human body, an observation that could be explained by suppression of afferent input during phonation. In this regard, it is noteworthy that the ventilatory response to breathing high CO2 is suppressed during speech (Phillipson et al. 1978).


    ACKNOWLEDGMENTS

We thank B. A. Recker for help in marking records and all of the subjects who participated in this study for their time, effort, and good cheer in the face of trying circumstances.

This work was supported by National Institute of Deafness and Other Communications Disorders Grant R01-DC01150 to L. O. Ramig, and by National Center for Voice and Speech Grant P60 DC-00976.


    FOOTNOTES

Present address and address for reprint requests: E. S. Luschei, 14719 N. E. 65th, Redmond, WA 98052.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 7 July 1998; accepted in final form 19 January 1999.


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0022-3077/99 $5.00 Copyright © 1999 The American Physiological Society




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