Electromyography and neurography in neurolaryngology

Journal of Voice Vol. 6, No. 2, pp. 15%187 © 1992 Raven Press~ Ltd., New York

Special Article

Electromyography and Neurography in Neurolaryngology M. Nasser Kotby, *E. Fadly, tO. Madkour, M. Barakah, A. Khidr, *T. Alloush, and M. Saleh Unit of Phoniatrics and *Department of Neurology, Faculty of Medicine, Ain Shams University; and ?Department of Neurology, Faculty of Medicine, Cairo University, Cairo, Egypt

Summary: Laryngeal electromyography (EMG) is an important tool in the study of laryngeal disorders. This review considers the current state of the art. The general principles of EMG and of the laryngeal neuromotor control system are reviewed. Important criteria for interpreting EMG characteristics, including the motor unit action potential and spontaneous activity, are considered in the context of several pathologic conditions. Technical and clinical difficulties are reviewed. Key Words: Electromyography--Potentials.

Section I. General Principles of Electromyography and Neurography

NEUROPHYSIOLOGICAL PRINCIPLES OF ELECTROMYOGRAPHY Normal findings in skeletal muscles During registration of the electrical activities of a normal skeletal muscle by needle electrodes, a series of phenomena are observed: 1. Insertion potentials are heard as brief discharges (300 ms) of single muscle fiber potentials on the insertion of the needle electrode (1). 2. If the muscle is completely relaxed, these initial transient potentials give way to complete electrical silence. 3. On attempted weak contraction, few motor units (the most excitable ones) are called into action and start to fire. The MUAPs are usually biphasic to triphasic in shape (2). The parameters of average normal MUAPs are 0.5-2 mV for amplitude and 5-15 ms for duration (2). Polyphasic potentials are seen normally and represent - 1 2 % of the MUAPs (3) (Fig. 1). 4. On increasing the strength of the contraction, these initial motor units increase their frequency of firing and new motor units are called into action. This recruitment increases until the baseline of the

ELECTROMYOGRAPHY Electromyography (EMG) is the study of electrical potentials generated in a skeletal muscle. EMG offers a useful tool for the study of activity of the skeletal muscles in vivo. It also provides a diagnostic tool that helps evaluate neurogenic and myogenic lesions of the skeletal motor system, and assists in monitoring the development and prognosis of these lesions. The diagnostic value of EMG is enhanced by the study of the condition of the motor and sensory nerves in response to electrical stimuli. The behavior of the nerves depends on the degree of the interruption of its course in the various lesions and pathologies. It may also provide indications of the restoration of function in a disrupted nerve. Address correspondence and reprint requests to Dr. M. Nasser Kotby, 11, E1 Ansary Street, Manshiet E1 Bakry, Cairo, Egypt.

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electromyographic screen is completely filled by the crowding MUAPs at maximal contraction. This stage is referred to as complete interference pattern (4) (Fig. 2). 5. Complete electrical silence returns on arrest of the contraction and resumption of full muscle relaxation. 6. MUAP parameters vary in different skeletal muscles. The average duration of signals in small muscles (e.g., facial and laryngeal muscles) is 4045% of that of skeletal muscles such as the biceps brachii. Also, the voltage output is 33% lower in the face than that of the biceps brachii (3).

ELECTROMYOGRAPHIC CHARACTERISTICS OF NEUROGENIC LESIONS Insertion activities are prolonged in duration. In addition, during complete relaxation there may be spontaneous activities in the form of the following.

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Fibrillation potentials These are of very short duration and amplitude (1.5 ms and 100 ~V) that fire at irregular waxing and waning rhythms. These fibrillation potentials represent the activity of individual muscle fibers mostly originating in the end plate region and are due to denervation (5) (Fig. 3). Positive denervation potentials These appear as biphasic potentials with initial positive (downward) deflection during rest with an average duration of 4.2 ms and average amplitude of 100 txV. They represent a pathognomonic feature of neurogenic lesion (1) (Fig. 4).

Fasciculations They are di- or tri-polyphasic potentials discharging arrhythmically and originating mostly from anterior horn cells. The duration and amplitude of fasciculations are similar to polyphasic motor unit potentials (6). On attempted contraction few MUAPs are recruited, showing prolongation of mean duration, increase in mean potential amplitude, and a greater proportion of polyphasic potentials (7) (Fig. 5). On maximal contraction the number of MUAPs does not increase significantly. The number recruited depends on the degree of the neurogenic lesion. Maximal recruitment of the MUAPs does not attain a complete interference pattern (4) (Fig. 6). Electromyographic characteristics of myogenic lesions

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Myopathy Insertion activities are increased. No spontaneous activity is detectable. The recruited MUAPs show reduction in the mean duration and a decrease

ELECTROMYOGRAPHY AND NEUROGRAPHY

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in the mean amplitude (8). The MUAPs show a high preponderance of polyphasic potentials with spiky components (9), accompanied by early recruitment and full interference pattern (6).

petitive stimulation (10/s) of a peripheral nerve (4). This reaction is seen in myasthenia gravis while in myasthenic syndrome there is initial increment in amplitude followed by decrement. This decrement in amplitude is characteristically observed in cases of Eaton-Lambert syndrome, mainly found as a complication of small-celled bronchogenic carcinoma (11), although it may be found in other conditions such as paramalignant or collagen disease.

Myotonia Myotonia shows spontaneous discharge of short, low-voltage potentials that look like fibrillation with typical waxing and waning of potential amplitude and discharge frequency causing the characteristic dive-bomber sound. This may or may not be accompanied by myopathic changes (4).

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Myositis Myositis shows a combination of denervation activity with myopathic changes (10). That is, spontaneous activity may be detected while MUAPs are of short duration and small amplitude with preponderance of polyphasic potentials.

A complementary part to electrodiagnosis is the study of the motor and sensory nerve conduction velocities, sometimes referred to as neurography. Nerve conduction velocity and motor evoked response For measurement of nerve conduction velocity, a kind of report on the status of the most rapidly conducting fibers in the nerve trunk, a supramaximal

Neuromuscular transmission defect There is a significant amplitude decrement (after 1 min) of the evoked response on supramaximal re.

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of broad polypbasic potentials in neurogenic lesions.

stimulus is applied to the nerve at two levels, provoking an e v o k e d potential, M response, in the muscle. The difference in latency of the two responses is the conduction time in the fast conducting fibers. The conduction velocity in that segment being the difference in latencies between the two points related to the distance in centimeters between the stimulated points. Nerve conduction and evoked electromyographic studies can help to localize the site of a peripheral nerve lesion together with determination of the degree of nerve injury, whether partial or complete (12). Slowing of nerve c o n d u c t i o n or a conduction block together with decrease in the motor response may occur at, or proximal to, the site of neuropraxis lesions (i.e., physiological nerve block), with normal nerve conduction in the distal fibers. Similarly, in early axonotmetic lesions (axonal interruption in which the connective tissue and Schwann cell base-

merit membrane remain intact 3-7 days after injury), there may be a drop in the conduction velocity proximal to the lesion. These cases will also show decrease in the amplitude of the evoked compound action potentials according to the percentage of the nerve fibers affected within the nerve trunk (13). In some pathological lesions the potential evoked in response to nerve stimulation may be dispersed, and thus has a much larger duration (4). This dispersion may be due to (a) slow duration in some fibers, (b) nonsynchronous firing of damaged nerve fibers after a single shock, or (c) collateral sprouting of surrounding nerve fibers in chronic partial denervation, thus leading to a dispersed polyphasic muscle response. In cases of neurotmetic lesions (complete nerve transection), there will be no nerve conduction and no motor response on stimulation of the nerve proximal to the lesion; normal conduction velocities may be present along the distal segment of the nerve until 7 days after nerve section (before Wallerian degeneration sets in).

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Journal of Voice, Vol. 6, No. 2, 1992

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Orthodromic stimulation The sensory nerve trunk is stimulated by a supramaximal short duration square wave stimulus applied distally. The nerve action potential is picked up by surface or subcutaneous needle electrodes at a proximal point. The latency time interval between stimulus and onset of nerve action potential is taken as the sensory fiber conduction time, which Lambert (14) believes arises from the motor end plate. Nerve action potentials have specific characteris-

ELECTROMYOGRAPHY AND NEUROGRAPHY

tics e.g., low amplitude, less than 5 IxV and polyphasic configuration (3). Slowing of the sensory conduction velocities may be selectively affected in conditions such as toxic neuropathies, vitamin B12 deficiency, and Friedreich's ataxia. Antidromic sensory conduction Antidromic sensory conduction is carried out by stimulating mixed nerves proximally and recording distally with submaximal stimuli (4). This is not typically used in the clinic. Somatosensory evoked responses Somatosensory evoked potentials (SEPs) are used in evaluating the proximal part of peripheral nerves where the application of conventional nerve conduction studies may be difficult (15). SEPs may offer more accurate information about the site (spinal or brain stem, thalamic or cortical) and the extent of the lesion than conventional nerve conduction studies (16). It also offers a tool for studying the condition of the central pathway.

REFERENCES 1. Buchthal F, Rosenfalck P. Spontaneous electrical activity of human muscle. Electroencephalogr Clin Neurophysiol 1966; 20:321-36. 2. Buchthal F. An introduction to electromyography in practice. Stuttgart, Germany: Georg Thieme Verlag, 1957:21-64. 3. Rodriguez AA, Oster YT. In: Licht S, ed. Electrodiagnosis and Electromyography. Wavery, 1971. 4. Ludin HP. Electromyography in practice. Stuttgart, Germany: Georg Thieme Verlag, 1980:21-64. 5. Jasper HP, Ballem G. Unipolar electromyograms of normal and denervated human muscle. J Neurophysiol 1949;12:231. 6. Goodgold J, Eberstein A. Electrodiagnosis o f neuromuscular diseases. Baltimore, MD: Williams & Wilkins, 1972:78121. 7. Buchthal F, Pinellie P. Action potentials in muscular atrophy of neurogenic origin. Neurology 1953;3:591. 8. Kugelberg E. Electromyography in muscle dystrophy. Neurol Neurosurg Psychiatry 1949;12:129. 9. PineUi P, Buchthal F. Muscle action potentials in myopathies with special regard to progressive muscular dystrophy. Neurology 1953;3:347. 10. Richardson AT. Clinical and EMG aspects of polymyositis. Proc R Soc M e d 1956;49:111-14. 11. Brown JC, Parry WC. In: Walton J, ed. Neuromuscular stimulation and transmission in disorders o f voluntary muscle. 4th ed. Edinburgh, Scotland: Churchill Livingstone, 1981:26. 12. Goodgold J, Eberstein A. Electrodiagnosis. Baltimore, MD: Williams & Wilkins, 1983:78, 121. 13. Hughes GB, Josey AF, Glasscock ME, Jackson CG, Ray WA, Simanis A. Clinical electroneurography. Statistical analysis of controlled measurements in twenty-two normal subjects. Laryngoscope 1981 ;91:1834--46. 14. Lambert EH. The accessory deep peroneal nerve. Neurology 1969;19:1169.

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15. Jones SJ. Clinical application of short latency somatosensory evoked potentials. Ann N Y Sci 1982;338:369-87. 16. Synck VM, Cowan JC. Somatosensory evoked potentials in patients with supraclavicular brachial plexus injury. Neurology 1982;31:1347-52.

Section II. Laryngeal Neuromuscular Control System Darley, Aronson, and Brown (1) have postulated that organized motor patterns are built into a hierarchy of six levels within the nervous system. These levels are integrated and interrelated. The higher levels function by activating, inhibiting, or modulating the patterns of the lower levels. The lowest level is organized into some reflexes that are integrated to perform purposeful movements. The six levels of the control of the motor act may be summarized as follows: 1. Lower motor neuron (bulbar): this is reflexive in nature 2. Vestibulo-reticular level: this regulates the lower motor neuron 3. Extrapyramidal level: this is responsible for the automatic subconscious control of activities and adjustment of muscle tone 4. Upper motor neuron (cortical-pyramidal): this initiates voluntary actions 5. Cerebellar: this is the error detector and error corrector; it controls the accuracy of the previous four levels 6. Conceptual programming level: the highest level. LARYNGEAL NEUROMUSCULAR HIERARCHY The laryngeal motor control system may be divided into the following levels. Cortical The efferent innervation of the larynx starts at the foot of the frontal precentral gyrus. The axons of the primary neurons run to the medullary centers via the corona radiata and travel in the internal capsule at the junction of the genu and the posterior limb. The fibers then descend mainly in the corticobulbar component of the pyramidal system. These fibers project on the bulbar nuclei for laryngeal control; that is, the nucleus ambiguous of both sides. The few large-diameter fibers (derived from cells in layer V of the inferior precentral gyrus) relay directly into the laryngeal motoneurons, while the many smaller diameter fibers derived from Journal of Voice, Vol. 6, No. 2, 1992

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smaller neurons in the inferior precentral and postcentral cortex relay indirectly through interneurons scattered through the laryngeal motoneuron pools. Most of these cortical projection fibers cross the midline within the pons and upper medulla oblongata, traversing the medial lemnisci on the way to enter the contralateral motoneuron pools, but some remain ipsilateral such that each cerebral cortex projects to the laryngeal motoneurons on both sides of the brain stem. Wyke and Kirchner (2) showed that the activity of the laryngeal motoneurons located in the nucleus ambiguous is influenced by projections that reach them from the cerebral cortex and from the mesencephalic tectum and cerebellum, as well as by reflexogenic inputs entering the lower brain stem from various receptor systems located within the larynx itself and within the lungs. Brain stem

The cell bodies of the second order neurons lie in the nucleus ambiguus in the caudal part of the brainstem. The cranial third of the nucleus ambiguous is considered to be the somata-motor center of the pharyngeal and some of the palatal muscles. These groups of muscles are closely related together in their central connections as well as in function. The center of the cricothyroid muscle is closely related to the pharyngeal and palatal muscles, thus illustrating how the cricothyroid muscle functionally incorporates with the external laryngeal muscles. The caudal parts of the nucleus ambiguus regulate the intrinsic laryngeal m u s c l e s a t t a c h e d to the arytenoid cartilage. All these muscles have been shown to act in intimate harmony (3). This segmental arrangement of the neuronal pools controlling the pharynx, palate, and larynx has been confirmed in the cat by Yoshida et al. (4--5). In one study they investigated the arrangement of motoneurons innervating the intrinsic laryngeal muscles using the horseradish peroxidase technique (4). After horseradish peroxidase injection into the cricothyroid, posterior cricoarytenoid, interarytenoid, and lateral cricoarytenoid muscles, labeled neurons were identified in the nucleus ambiguus ipsilaterally. The motoneurons for the cricothyroid were found ipsilaterally in the retrofacial and ambiguus nuclei. The labeled cell column of cricothyroid was located much more rostra! than the others. The labeled cell columns of the other laryngeal muscles, except cricothyroid, differ slightly from each other and are arranged more cauJournal of Voice, Vol. 6, No. 2, 1992

dally in the order of posterior cricoarytenoid, thyroarytenoid, lateral cricoarytenoid, and interarytenoid. In the nucleus ambiguus, the motor neurons of the cricothyroid showed compact form and were located in the ventral part, those of the posterior cricoarytenoid were aggregated and occupied the middle part, those of the thyrorarytenoid were scattered and were seen in the dorsal part, and those of the lateral cricoarytenoid and interarytenoid were sparse and were recognized widely in the nucleus. The same authors demonstrated also that the motoneurons of the pharyngeal, cervical esophageal, and laryngeal muscles were arranged in that order rostrocaudally. The motoneurons of cricothyroid are closer to the motoneurons of the pharyngeal muscles than those of the other laryngeal muscles. This is understandable because the cricothyroid is phylogenetically derived from the inferior constrictor of the pharynx. The motoneurons of the laryngeal muscles of monkeys are arranged similarly in a rostracaudal pattern (6). Peripheral nerves The vagus nerve emerges from the medulla oblongata between the olive and inferior cerebellar peduncle. It presents two enlargements: the jugular (superior) and nodose (inferior) ganglia, at the level of the jugular foramen shortly after it emerges into the neck through the foramen. These ganglia contain the first order neurons in the afferent pathways of the vagus nerve, including the larynx. The cranial accessory nerve communicates with the superior (jugular) ganglion and joins the main trunk of the vagus just distal to the inferior or nodose ganglion, its motor fibers being distributed through the pharyngeal and recurrent laryngeal branches of the vagus nerve (7,8). In the neck the vagus nerve has several branches that control the voice and speech mechanism. These branches are the pharyngeal nerve, superior laryngeal nerve and its two branches (internal and external laryngeal nerve), and the recurrent laryngeal nerve. Pharyngeal nerve

The pharyngeal nerve emerges from the upper part of the inferior (nodose) ganglion of the vagus. It descends to the level of the middle pharyngeal constrictor muscle. At that point, it divides into filaments that receive branches from the sympathetic trunk and glossopharyngeal and external laryngeal nerves to form the pharyngeal plexus. The plexus

ELECTROMYOGRAPHY AND NEUROGRAPHY

provides nerve fibers to the pharynx and to all the muscles of the soft palate except the tensor palati muscle. Superior laryngeal nerve It emerges from the inferior ganglion and descends along the pharynx. About 2 cm below the inferior ganglion it divides into two branches. Internal laryngeal nerve. The internal laryngeal nerve descends to the level of the thyrohyoid membrane where it pierces and enters it as a neurovascular bundle just in front of the ligament between the greater cornu of the hyoid bone and the upper horn of the thyroid cartilage. The nerve divides into two additional branches. Both contain afferent fibers from the mucous membrane that lines the larynx above the level of the vocal folds. They also contain fibers from muscle spindles and other stretch receptors in the larynx. External laryngeal nerve. This motor efferent branch of the superior laryngeal nerve descends posterior to the sternohyoid muscle. It supplies the cricothyroid muscle and the inferior constrictor of the pharynx. Recurrent laryngeal nerve The right recurrent laryngeal nerve arises from the vagal trunk in front of the right subclavian artery. It loops under the artery from front to back and ascends along the trachea behind the common carotid artery (9). The left recurrent nerve arises from the vagal trunk deep to the arch of aorta, winding under it from front to back. It ascends lateral to the trachea to reach the tracheoesophageal groove in the neck. The right and left recurrent laryngeal nerves after reaching the tracheoesophageal groove ascend in that groove to enter the larynx behind the cricothyroid joint on either side. Both right and left recurrent laryngeal nerves supply all the intrinsic laryngeal muscles except the cricothyroid. They also supply sensory filaments to the mucous membrane lining the larynx below the level of the vocal folds and they carry afferent fibers from stretch receptors in the intrinsic laryngeal muscles. The recurrent nerves may enter the larynx unbranched or they may divide into two to six branches at variable distances from the cricothyroid joint (10). In most cases, the nerve divides into two main branches, an anterior and posterior branch. The latter was thought to supply the abductor fibers (11). However, the extralaryngeal division of the recurrent nerve is divided into motor and sensory branches (12).

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In their anatomical study of laryngeal nerve pathways, Kotby et al. (13) demonstrated how the trunk of the recurrent laryngeal nerve divided into two terminal branches before reaching the inferior constrictor muscle in 73.3% of 30 larynges. They also found that the anterior (lateral) division always inn e r v a t e d the lateral c r i c o a r y t e n o i d and thyroarytenoid. In 13.3% of their specimens, this nerve innervated the posterior cricoarytenoid muscle as well, and in 3% of the specimens it gave an anastomotic branch to the internal branch of the superior laryngeal nerve. In 86% of the larynges, 6% of the posterior (medial) division innervated the posterior cricoarytenoid and interarytenoid muscles, and gave an anastomotic branch to the internal branch of the superior laryngeal nerve. In 13.3% of the specimens, it did not provide any m u s c u l a r branches, and continued as the sensory anastomotic branch to the branch of the superior laryngeal nerve.

FIBER TOPOGRAPHY IN THE NERVE TRUNK There have been several attempts to describe a fixed pattern of arrangement of nerve fibers in the recurrent nerve trunk. The fibers supplying the posterior cricoarytenoid muscle have been thought to occupy a peripheral position (14). The work of Sunderland and Swaney (15) on the internal topography of the recurrent nerve failed to confirm any constant pattern. They found that the nerve bundles were not arranged in parallel strands, but there was an intermingling of fibers from different fasciculi. Likewise, Kotby et al. (13) reported that the fasciculi of the nerve intermingled with each other, and that the fiber sizes of the recurrent nerve and its divisions were bimodal in pattern.

NERVE FIBER SPECTRUM

Wyke and Kirchner (2) using anatomical and physiological studies in the cat, dog, monkey, and human showed that the laryngeal motor nerve fibers vary widely in diameter, but in general are somewhat smaller than those innervating striated muscles elsewhere, with most of them being between 6 and 10 ixm in diameter (but a few as large as 20 jxm). This correlates with the fact that conduction velocity of most laryngeal motor nerve fibers is slower Journal of Voice, Vol. 6, No. 2, 1992

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(-50--65 m/sec) and that their refractory periods are longer, compared with the majority of nerve fibers supplying motor units of limb muscles. Traditional nerve fiber degeneration methods (16) applied after intracranial transection of the vagus nerve in the cat indicated that (a) most of the fibers of the recurrent laryngeal nerve are motor (alpha) fibers, (b) most of the motor fibers leave the brainstem in the most rostral rootlets of the vagus nerve, and (c) motor fibers to the larynx form a discrete bundle within the trunk of the vagus nerve before forming the recurrent laryngeal nerve. Using HRP tracer, the authors (16) showed diffuse arrangement of both adductor and abductor nerve fibers in the vagus trunk, but collection of these fibers into adductor and abductor fibers in the recurrent laryngeal nerve occur before entering the larynx. The diffuse arrangement of these fiber groups explains the usually mixed functional results obtained after reimplantation of the recurrent laryngeal nerve into a laryngeal muscle. Mitchell (17) showed that the laryngeal nerves also contain small-diameter vasomotor and secretomotor fibers of sympathetic (superior and middle cervical ganglia) and parasympathetic (dorsal nucleus of the vagus).

Motor end plate On approaching the muscle fibers the motor nerve fiber loses its myelin and schwann sheaths and comes into close contact with the sarcoplasm. At this level the cytoplasmic membrane creases into a particular structure called the subneural apparatus (18). Laryngeal muscle fibers show more than one end plate, large and small, located at various unfixed sites, in many cases at one end of the fiber. The nerve fibers supplying the small end plates, without a characteristic subneural apparatus, have been found to be of a thin caliber (19), an arrangement suggesting a similarity to the intrafusal muscle fibers of the gammamotoric system. Rudolph (20) has observed muscular fibers of the vocal muscles presenting up to five separate neuromuscular junctions. The proportion of such fibers was estimated to be 20%. Similarly, from two thirds to three quarters of the muscle fibers of some extraocular muscles in humans have two or more motor end plates (21). Rossi and Cortesina (22) found that the proportion of muscular fibers with multiple innervation reached 5% in the posterior cricoarytenoid muscle. It has also been indicated that the majority of type I muscle fibers have multiple motor end plates, Journal of Voice, Vol. 6, No. 2, 1992

while the majority of type II fibers have single motor end plates (23). In the thyroarytenoid muscle Sonesson (24), using histochemical examination, found that the end plates were seen to be concentrated in a single zone, situated equidistant from the arytenoid and thyroid cartilage, and perpendicular to the vocal ligament.

Motor unit The fibers of the recurrent nerve end on a small number of muscle fibers, which have been estimated to range from as low as two to three fibers per unit (18,25) to a midrange of up to 30 (2,26) to a high number of muscle fibers in the motor unit ranging from 116 to 247. The low innervation ratio is striking when compared with other skeletal muscles, which may have up to 2,000 fibers per unit. This neuromuscular arrangement of the laryngeal muscles is suitable for the action required from these muscles: they are known to be non-weight bearers and to perform delicate actions, entailing rapid contractions (3). Although small motor units are generally inner.. vated by finer diameter nerve fibers than are large motor units, the marked differences in the contraction characteristics of the individual intrinsic laryngeal muscles, in response to stimulation of their motor fibers in the laryngeal nerves, probably reflect differences in the functional properties of their contained muscle fibers (or of their neuromuscular junction) rather than major differences in the diameter of their related motor nerve fibers (2). Muscle fiber type and contraction properties The morphological arrangement of the muscle fibers in different internal laryngeal muscles presents various patterns. Some fibers run directly between the points of attachment, others end on intermediate tendons or on perimysium of other muscle fibers. This arrangement holds true for all of the internal laryngeal muscles (19), although Rossi and Cortesina's (22) work illustrates differences between the posterior cricoarytenoid muscle and the adductor group. Their observation of adduction muscles consisted only of fibers running from one insertion to the other, contrary to Zenker's (19) study of the vocalis muscle. In the thyroarytenoid muscle Sonesson (24), using histochemical examination, found that the musculotendinous junctions of the muscle fibers were

ELECTROMYOGRAPHY AND NEUROGRAPHY

identified by the occurrence of cups at the muscle fiber ends, which were found anteriorly at the inner aspect of the thyroid cartilage and posteriorly at the arytenoid cartilage. No muscle fiber ends could be seen along the vocal ligament or throughout the length of the vocal muscle. Graduation in physical properties of the internal laryngeal muscles has been described: the vocalis muscle is the fastest contracting muscle, the posterior cricoarytenoid has the slowest and most sustained contraction; the cricothyroid occupies an intermediate position (27-29). This reflects an equivalent variation of the type of metabolism of these muscles. The slow, sustained contraction of the posterior cricoarytenoid muscle demands a high aerobic metabolism, and has been found to have a rich capillary blood supply and a high density of mitochondria. On the other hand, the fast muscle has both aerobic and anaerobic types of metabolism (30). Thus, contractional properties demonstrate different degrees of activity of the individual members of the internal laryngeal muscles (31). Dubowitz and Brooke (32) distinguished two groups: type I slowly contracting and type II rapidly contracting fibers. They further subdivided type II fibers into subgroups II A, II B, and II C according to their ATPase reaction. Kersing (33) studied the histological and histochemical features of the vocal musculature in humans and animals. He distinguished two broad groups: type I slowly contracting; and type II rapidly contracting fibers. Of particular interest are the developmental differences in muscle fibers. The majority of the muscle fibers of the vocal musculature of infants are shown to be immature and poorly differentiated; most are type II fibers with type II C preponderance. By adulthood the vocal musculature displays most of the characteristics of skeletal muscle in other parts of the body of the same subject, although there is more peri- and endomysial connective tissue than in other skeletal muscles. The type I/type II relationship corresponds to that of the skeletal muscles. No sex differences could be found other than those that were simply a function of the mass of the laryngeal skeleton and its associated muscles. In old age the endomysial connective tissue increases and the fascicular architecture disappears with the appearance of areas with low mitochondrial enzyme activity. Brondbo and his colleagues (34) described the histochemistry of canine posterior cricoarytenoid muscle, diaphragm, sternothyroid, and sternomas-

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toid muscles. They found that the muscle fiber type composition in the posterior cricoarytenoid, diaphragm, and sternothyroid muscles differed very little and showed a slightly type II preponderance. These investigators (35) also described the histochemical examination of the human posterior cricoarytenoid muscle and diaphragm from laryngectomized persons and heart donors, respectively. They found that the mean fiber type pattern of the posterior cricoarytenoid muscle was 57% type I, 36% type II A, and 7% type I I B as compared with 42% type I, 42% type II A, and 16% type II B in the diaphragm. Both muscles were characterized by a great oxidative capacity. Laryngeal afferent system The sensory outflow from the larynx above the level of the glottis is achieved by superior laryngeal nerve fibers. The recurrent laryngeal nerve carries sensory stimuli from the larynx, below the level of the vocal fold. A number of sensory receptors have been described in the laryngeal structures of mammalian species. These are mucosal touch receptors and mechanoreceptors in the joint capsule, as well as in the deeper structures of the larynx (36). AbouE1-Enein and Wyke (37) and Wyke and Kirchner (2) showed that the mechanoreceptors in the larynx are of two types, articular mechanoreceptors of phasic excitation and the receptors responsible for the myotatic reflexes. Muscle spindles have been negated in the intrinsic laryngeal muscles. It has even been thought that the intrinsic muscles, being non-weight bearers, are simple in action and hence have very little proprioceptive properties. This is contradictory to the consistent finding of resting postural activity in these muscles (38-41) and to the demonstrated presence of muscle spindles in intrinsic laryngeal muscles of humans and animals (42-44). Moreover, in a histologic examination of the adductors and tensors of the vocal folds, Baken (44) and Baken and Naback (45) found that the thyroarytenoid, interarytenoid, and lateral cricoarytenoid contained several spindles. The spindles observed in the intrinsic muscles ranged from 1,200 to 3,600 ~m in length and had from three to nine intrafusal fibers. However, they were unable to identify any spindle structures in the cricothyroid muscle. It is now well established that each of the intrinsic laryngeal muscles (in cats and humans) contain a few small muscle spindles even as spiral endings, although they appear to be more numerous in huJournal of Voice, Vol. 6, No. 2, 1992

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mans than in other species. The spectra of fiber diameter of the inferior laryngeal nerve and the external laryngeal nerve include fiber sizes on the same order as those of the fusimotor nerve fibers (1-6 Ixm) (gamma system) found in muscle nerves in other parts of the body. REFERENCES 1. Darley FL, Brown JR. Motor speech disorders. Hierarchy of motor organization. Philadelphia, PA: Saunders, 1975. 2. Wyke BD, Kirchner JA. Neurology of the larynx. In: I-Iinchcliffe, Harrison, eds. Scientific foundations of otolaryngology. London: William Heinemann Medical Books Ltd, 1976, 546-74. 3. Kotby MN, Haugen LK. The mechanics of laryngeal function. Acta Otolaryngol 1970;70:203-11. 4. Yoshida Y, Miyazaki T, Hirano M, Shin T, Kanasaki T. Arrangement of motoneurons innervating the intrinsic laryngeal muscles of cats as demonstrated by horseradish peroxidase. Acta Otolaryngol 1982;94:329. 5. Yoshida Y, Miyazaki T, Hirano M, Shin T, Kanasaki T. Topographic arrangement of motoneurons innervating the suprahyoid and infrahyoid muscles. A horseradish peroxidase study in cats. Ann Otolaryngol Rhinol Laryngol 1983 ;92: 3. 6. Yoshida Y, Mitsumasu T, Miyazaki T, Hirano M, Kanasaki T. Distribution of motoneurons in the brain stem of monkeys, innervating the larynx. Brain Res Bull 1984;13:443. 7. Bowden REM. Innervation of intrinsic laryngeal muscles in ventilatory and phonatory control system. In: Wyke BD, ed. International symposium. London: Oxford University Press, 1973:370-8. 8. Dixon DR, Maue-Dixon W. Anatomical and physiological bases of speech. Boston: Little, Brown, 1982:338. 9. Warwick R, Williams PL, eds. Gray's anatomy. 35th ed. London: Longman, 1973. 10. Bowden REM. Surgery of the recurrent laryngeal nerve. Proc R Soc Med 1955;48:437. 11. Cracovdner AJ. Quoted from Kaplan HM (1954). Anatomy and physiology of speech. New York: McGraw-Hill, 1960. 12. Williams AF. The recurrent laryngeal nerve and the thyroid gland, d Laryngol 1954;68:719. 13. Kotby MN, Abdel Rahman S, El Sammaa M. Observations on the pattern of the terminal branching of the recurrent laryngeal nerve and its internal nerve and its internal topography. Proceedings of the Fourth Annual Ain-Shams Medical Congress. Ain-Shams University, Cairo, Egypt, 1980. 14. Seman F. Proclivity to diseases of the abductor Fibres. J Laryngol 1881;2:197. 15. Sunderland S, Swany WE. The intraneural topography of the recurrent laryngeal nerve in man. Anat Rec 1952;114: 411. 16. Gacek RR, Malmgren LT, Layon MI. Localization of adductor and abductor motor nerve fibers of the larynx. Otol 1977;86:770. 17. Mitchell GAG. The autonomic nerve supply of the throat, nose and ear. J Laryngol 1954;68:495. 18. Piquet J, Barets A. Observations sur l'innervation motoric du muscle vocal. Acta Otolaryngol (Stockh) 1960;51:203. 19. Zenker W. Vocal muscle fibers and their motor end-plates. In: Brewer DW, ed. Research potentials in voice physiology. State University of New York, 1964:7. 20. Rudolph G, Particularites des synapses neuro-musculaires

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21. 22. 23.

24.

25. 26. 27.

28. 29. 30. 31.

32. 33.

34.

35.

36.

37. 38.

39.

40. 41. 42. 43.

44. 45.

dans le muscle vocal de l'homme. Rev laryngol Otol Rhinol (Bord) 1962;83:569. Kupfer C. Motor innervation of the extraocular muscle. J Physiol (LoncO 1960;153:522. Rossi G, Cortesina. Morphological study of the laryngeal muscles in man. Acta Otolal~ngol (Stockh) 1965;59:575. Bendiksen FS, Dahl HA, Teig E. Innervation of muscle fibers in the human thyroarytenoid muscle. Acta Otolaryngol 1981 ;91:391. Sonesson B. On the anatomy and vibratory pattern of the human vocal folds. Acta Otolaryngol [Suppl] (Stockh) 1960; Suppl. 156:80. English DT, Blevins CE. Motor units of laryngeal muscles. Arch Otolaryngol 1969;39:779. Rudi L. Some observations on the histology and function of the larynx. J Laryngol 1959;73:1. Hast MH. Physiological mechanisms of phonation: tension of the vocal fold muscle. Acta Otolaryngol (Stockh) 1966; 62:309. Hast MA. Mechanical properties of the vocal fold muscles. Practice Laryngol 1967;29:53. Hast MA. The respiratory muscle of the larynx. Ann Otolaryngol 1967;76:489. Mira I, Vidi I. Stuttura del musculo vocal uome e toria neuro chronassica della. Arch J Otolaryngol 1966;77:531. Kotby MN, Hagen LK. Attempts at evaluation of the function of various laryngeal muscles in the light of muscle. Acta Otolaryngol 1970;70:419-27. Dubowitz V, Brooke MH, Neville HE. Muscle biopsy: a modern approach. Philadelphia, PA: Saunders, 1973, Kersing W. De Stembandmusculatuur een histologische en histochemische studie. Drukkerij Elinkwijk BV-Utrecht~ 1984. Brondbo K, Dahl HA, Teig E. The histochemistry of the posterior crico-arytenoid (PCA) muscle in the dog, compared with the diaphragm, the sternohyoid, and the sternomastoid muscle. Acta Otolaryngol 1985;100:289. Brondbo K, Dahl HA, Teig E, Gujord KM. The human posterior cricoarytenoid (PCA) muscle and diaphragm. Acta Otolaryngol 1986;102:474. Eyzaguirre C, Sampson S, Tylor R. The motor control of intrinsic laryngeal muscles in the cat. In: Grantit R, ed. Nabel symposium 1. Muscular afferents and motor control. Stockholm: Amquist & Wiksell, 1966. Abo-El Enein MA, Wyke B. Laryngeal myotatic reflexes. Nature 1966;209:682. Faaborg-Andersen K. Electromyographic investigation of intrinsic laryngeal muscles in humans. Acta Physiol Scand [Suppl] 1957;41:140. Kotby MN, Haugen LK. Critical evaluation of the action of the posterior cricoarytenoid muscle, utilizing direct E M G Study. Acta Otolaryngol 1970;70:260-8. Kotby MN. Electromyography of the laryngeal muscles [Thesis]. Cairo, Egypt: Ain Shams University, 1967. Haglund S. The normal electromyogram in human cricoarytenoid muscle. Acta Otolaryngol (Stockh) 1973 ;75:448. Lucus Knee MF. Muscle spindles in human laryngeal muso cles. J Anat 1961;95:25. Branconi R, Molinari G. Electromyographic evidence of muscle spindles and other sensory endings in the intrinsic laryngeal muscles of the cat. Acta Otolaryngol 1962;55:253. Baken RJ. Neuromuscular spindle in the intrinsic muscles of a human larynx. Folia Phoniatr (Basel) 1971 ;23:204. Baken RJ, Naback CB. Neuromuscular spindles in intrinsic muscles of a human larynx. J Speech Hear Res 1971;14:513,

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S e c t i o n III. N e u r o l o g i c a l D i s o r d e r s o f the Larynx The main role of laryngeal EMG and neurography is the detection and evaluation of diseases of the neuromuscular system of the larynx. Thus, they are most useful as a diagnostic aid in neurological disorders of the larynx. An outline of these disorders is given in order to highlight the potentials of EMG and neurography in the diagnosis and management of this type of laryngeal ailment. The neuromuscular systems of the larynx may break down on the motor (efferent) or sensory (afferent) level. In clinical practice, the motor breakdown is more readily noticed, but the sensory disorders are also of considerable interest. LARYNGEAL SENSORY DISORDERS Detailed description of some neurologic entities of laryngeal sensory disorders have been described, including anesthesia, and hyper- and paresthesia (1). Laryngeal anesthesia is noticed frequently with laryngeal tuberculosis (2), a disease that is becoming infrequent. Hyper- and paraesthesias are sometimes referred to as "abnormal sensations in the throat" (3). Frequently clinicians interpret these feelings as a part of the syndrome of phonasthenia (4). The hyperirritable larynx with frequent episodes of laryngeal spasms may be considered a sensory problem that initiates a reflex motor reaction. This ailment may be encountered in some hyperfunctional voice disorders. In a similar way, abnormal afferent stimuli may be an etiological factor in the obscure condition of spastic dysphonia (5). EMG and neurography have limited application in the evaluation and follow up of these sensory disorders of the larynx. Laryngeal motor disorders On the other hand, in motor neurological disorders EMG and neurography may play a prominent role in both diagnosis and prognosis. The breakdown in the laryngeal motor control system may be at the level of lower motor neuron (LMN) or upper motor neuron (UMN). L o w e r motor neuron l e s i o n s

Lower motor neuron lesions of the larynx can cause flaccid (bulbar) dysarthrophonia (6). The

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level of the breakdown may be at (a) the muscles (muscular dystrophies, myotonias, and myopathies); (b) the neuromuscular junction (myasthenia gravis); or (c) the peripheral nerve systems (main trunk vagus, inferior laryngeal, superior laryngeal). The affection of these nerves may be at the posterior fossa, intracranially, or at the skull base (jugular foramen), neck, or mediastinum and pulmonary apex. Several syndromes result from combinations of cranial nerve lesions in the posterior fossa and jugular foramen: 1. Affection of nerves IX, X, and XI in the jugular foramen (Vernet's syndrome). 2. Affection of nerves X and XI (Schmidt's syndrome). 3. Affection of nerves X, XI, and XII (Hughling Jackson syndrome). 4. Affection of nerves IX, X, XI, and XII (Collet Sicard syndrome). 5. Affection of nerves IX, X, and XII, and Horner's syndrome (7). Upper motor neuron lesions (Dysarthrophonias)

Breakdown in the higher motor control systems (6,8,9) may lead to several types of dysarthrophonia: 1. Pyramidal (bilateral lesions); causing spastic dysarthrophonia. 2. Amyotrophic lateral sclerosis (upper and lower neuron lesions) causing mixed flaccid-spastic dysarthrophonias. 3. Extrapyramidal lesions, including Parkinson disease with hypokinetic constant dysarthrophonia, chorea with hyperkinetic dysarthrophonia, and Dystonia (athetosis) with hyperkinetic fluctuating dysarthrophonia. 4. Cerebellar lesions causing ataxic dysarthrophonia. Unclassified neurological ailment. This group may include spastic dysphonia (5,10), organic (essential) voice tremors, palatopharyngeal myoclonus, Gilles de la Tourette syndrome, and stuttering. Although not a primary laryngeal problem, some investigators have studied the laryngeal behavior during stuttering and considered the laryngeal phenomenon as an important part of the ailment. Further work is needed to determine the role of the larynx. Functional dysphonias. These dysphonias may be of habitual origin, or psychogenic origin, as suggested by Kotby (4,11). Apraxic dysphonia. This encompasses a wide variety of lesions affecting central control of language. Journal of Voice, Vol. 6, No. 2, 1992

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It may be associated with dysphasia (12) or dyspraxia. Automatic movements of blowing, coughing, and so forth are present while volitional phonatoarticulatory activities are disrupted.

Laryngological outcome Motoneurological laryngeal afflictions reflect mainly on the integrity of movements of the vocal folds. The breakdown may be exhibited as a complete loss of movement of one or both vocal folds, restriction of the gross adduction-abduction movement of one vocal fold leading to clear asymmetry of glottic movement in range and timing. Wendler et al. (13) observed that the paralyzed vocal fold adopted the paramedian position in 75% of the 1,087 cases examined, whereas the intermediate position was adopted in 16% and the median position in only 9% of the cases. Dejonckers (14) found similar results and stated that in cases of denervation of a vocal fold, the paramedian position was significantly more frequent than all the other positions. The fine vibratory movements of the vocal folds may be subtly affected in various ways depending on the site and severity of the lesion. Some of the subtle changes can be observed with stroboscopy. For example, the stroboscopic glottal wave may be modified by less vertical displacement of the mucosal "wave flutter" and reduced amplitude. In milder and recovering cases, variations and asymmetry in amplitude, phase, glottic wave, and degree of glotted closure may be noticed when patients are followed across time. Because vocal fold mobility disturbance is the main sign of neurological ailment of the larynx, the position of the paretic vocal fold is considered to be important for making the diagnosis and planning management. Certain fixed positions have been unjustifiably designated to certain pathological entities that may mislead the clinician into making incorrect diagnoses. However, the immobile vocal fold may adopt several positions not only dependent on the type of the nerve-muscle affection but also dependent on the degree of that affection, and on the anatomical peculiarities of the muscles (15,16) and joint (17). Accordingly, for the evaluation of a neurological disturbance of the larynx manifested by a vocal fold mobility problem, it may be necessary to describe the presence, range, and side of residual movement, the position and configuration of an immobile vocal

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fold as judged by its distance from the middle line posteriorly (a microscopic grid may be helpful in measuring this distance in indirect microlaryngoscopy), and stroboscopic movements of the affected vocal fold(s), which may show some variation in glottic wave, amplitude, timing, and degree of glottic closure. Despite the help the clinician may get from visual evaluation of laryngeal movement a vocal mobility disorder case cannot be diagnosed with precision (cause, degree, and distribution of the lesion) using videostroboscopy alone. Insight into the neuromuscular status (by EMG and neuromyography) are essential for diagnosis and prognosis. REFERENCES 1. Thomson St C, Negus VE, eds. Diseases o f the nose and throat. 6th ed. Part VII. London: Cassell, 1955. 2. Musgrove J. Nervous diseases of the larynx. In: ScottBrown WG, ed. Diseases o f ear, nose and throat. London: Butterworth, 1952:544. 3. Hirano M. Personal communication, 1985. 4. Kotby MN. Voice disorders, recent diagnostic advances. J Otolaryngol (Egypt) 1986;3:69-98. 5. Valancien B. Neuro-psychiatric aspects of spastic dysphonia (quoted in Bloch P). Folia Phoniatr 1965;17:301-64. 6. Aronson AE. Voice disorders, an interdisciplinary approach brain. New York: BC Decker, 1980. 7. Howard D. Neurological effections of the pharynx and larynx. In: Ker AG, ed. Scott-Brown's otolaryngology. Laryngology. 5th ed. Stoneham, MA: Butterworths, 1987. 8. Darley FL, Aronson AE, Brown JR. Differential diagnostic patterns of dysarthria. J Speech Hear Res 1969;12:246-369. 9. Darley FL, Aronson AE, Brown JR. Motor speech disorders. Philadelphia: Saunders, 1975. 10. Bloch P. Neuro-psychiatric aspects of spastic dysphonia. Folia Phoniatr 1965;17:301-64. 11. Kotby MN. Voice disorders: recent diagnostic advances. In: Myers E, ed. New Dimensions in otorhinolaryngology and head and neck surgery. Amsterdam: Elsevier, 1985;1:33740. 12. Lauria AR. Traumatic aphasia, its syndromes, psychology and treatment. The Hague, The Netherlands: Movton, 1970. 13. Wendler J, Vollprecht I, Notzel M, Klein K, Fuchs R. Stimmlippenlahmungen in der phoniatrische praxis. Folia Phoniatr 1984;36:74-83. 14. Dejonckere PH. EMG o f the larynx. Louvain, Belgium: University of Louvain, 1987. 15. Mossallam I, Kotby MN, Abd E1 Rahman S, E1 Samma M. Attachment of some internal laryngeal muscles at the base of the arytenoid cartilage. A cta Otolaryngol (Stockh) 1987; 103: 649-56. 16. Zemlin WR, Darvis P, Gaza C. Fine morphology of the posterior cricoarytenoid muscle. Folia Phoniatr 1984;36:23340. 17. Mukasa T, Ueda T. The position of the vocal cord in cadaver and so called cadaveric position of the vocal folds. J Otolaryngol (Tokyo) 1962;62:184-92.

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Section IV. Principles of Laryngeal Electromyography HISTORY AND ARMAMENTARIUM The first attempt in the field of laryngeal electromyography was made by Weddell et al. in 1944 (1). They suggested that in order to record the action potentials from the intrinsic muscles of the larynx, it was necessary to use a concentric needle electrode of sufficient length, so that all manipulations could be carried out through a laryngoscope. The new test was applied by Feinstein (2) and Macbeth (3) in their studies on vocal cord paralysis, and further developed along three main lines (4). APPROACHES

Direct approach through a surgically performed pharyngostoma or laryngofissure Several investigations have been conducted to study the action potentials of laryngeal muscles using concentric or bipolar needle electrodes inserted directly in the muscle through a surgically established route. This method of insertion is not common, but is of historical interest (5-7). Greiner et al. (8) compared recordings obtained by this direct approach and by the transcutaneous approach, and found them similar. Natural approach through direct or indirect laryngoscopy Direct laryngoscopy approach After the early works of Weddell et al. (1), Feinstein (2), and Macbeth (3), several other workers adopted this technique. Kotby and Haugen (9) studied the activity of the posticus muscle by the direct approach using neuroleptic analgesia, which allows active cooperation of the patient with the operator. The neuroleptic was supplemented by topical pharyngolaryngeal analgesia using Lidocaine spray. The authors recommended that the first session in laryngeal electromyographic investigations should be performed in the endoscopy theater, and followup examinations performed in the EMG clinic through percutaneous route. Shipp et al. (10) also used this method because direct laryngoscopy offers greater maneuverability and better illumination of the laryngeal structures than indirect laryngoscopy.

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Indirect laryngoscopy approach Indirect mirror laryngoscopy. Faaborg-Andersen (11), in his fundamental and now classical study on laryngeal EMG, managed to reach all the small internal laryngeal muscles by needle electrodes passed through the mouth and secured in place via an indirect mirror laryngoscopy. However, the cricothyroid muscle was approached transcutaneously, Equipment has been specifically designed for indirect mirror laryngeal EMG: laryngeal forceps (12) and the L-shaped probe developed by Hirose (13). Indirect telescopy. Magnification of the structures enhanced clinicians' insertion abilities. Kittel et al. (14) used the magnifying telescope successfully for inserting microelectrodes into various laryngeal muscles of the waking patients; Thumfart (15,16) used the 300 endoscope, developed by von Stuckrad (17), for precise transoral electrode insertion, using a technique similar to that for removing specimens from the larynx for histological investigation. The basic tool for laryngeal EMG, according to Thumfart's method, was the electrode-holding forceps with either bipolar needles or hooked-wire electrodes. Percutaneous approach, through the soft tissue overlying larynx. Fink et al. (18) first described the percutaneous technique of electrode placement in the laryngeal muscles. The muscles tested, the cricothyroid and the thyroarytenoid, were identified by reference to their points of attachment to the laryngeal skeleton. Greiner et al. (8) improved on this percutaneous technique, while Kotby (4,19) provided a detailed description of how to execute the percutaneous technique of laryngeal EMG. In his attempt to standardize the technique he named three standards of critical value for proper electrode placement: the site of cutaneous puncture, the angle the electrode makes with the plane of the front of the neck, and the distance it must penetrate from the surface. He stressed that all manipulations should be performed submucosally, because if the needle penetrates the unanesthetized mucosa, a bout of coughing or a laryngeal spasm may be initiated. In examination of the interarytenoid muscle, where the needle must traverse the laryngeal lumen, topical analgesia may be required. Also, a sedative administered half an hour before testing in exceptionally anxious subjects was found to be helpful. Apparatus and technique The electromyograph is composed of an electrode system which feeds the electrical sign into a

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preamplifier and differential amplifier. The output of the amplifier is connected to a cathode ray oscilloscope, a loudspeaker, and a write-out system.

Electrodes Two types of electrodes may be used, either surface electrodes or needle electrodes. Surface electrodes. These electrodes pick up electric activity from a wide area. In this way, the signal represents the global activity of all muscle fibers in the area. Such electrodes are easy to apply and cause no discomfort to the patient. The main disadvantage, particularly in case of the small laryngeal muscles, is that one does not know exactly which muscle's activity is picked up. Nevertheless, surface electrodes may be useful in recording "general laryngeal area" muscle tension in order to develop a biofeedback control, as in cases of hyperfunctional dysphonia (20). Needle electrodes. Monopolar electrodes are those formed of an insulated metal with a bare tip, working in conjunction with a large area reference electrode. Some clinicians find the presence of inherent technical problems in the unipolar electrodes (21,22) unacceptable. Unipolar concentric needle electrodes are those with a central pole (wire) cemented into the lumen of a hypodermic needle. The second pole is formed by the free tip of the sheath of the cannula. Dedo and Hall (23) stated that concentric needle electrodes pick up a significant amount of "cross talk" potentials from nearby muscles. When used in intrinsic laryngeal EMG, they were found to be constantly recording potentials from muscles over 0.5 cm distance from the recording electrode. On the other hand, experiments performed by Kotby and Haugen (9) showed that simultaneous recordings from the thyroarytenoid and ipsilateral posterior cricoarytenoid muscles failed to demonstrate synchronization of the MUAP recorded from the two muscles. Pollak (24) stated that the amplitudes and wave shapes of the signals obtained by a coaxial (concentric) needle are not significantly different from those obtained by a monopolar needle. However, the coaxial needle picks up much less noise due to the relatively small spacing between its electrode poles. Bipolar concentric needle electrodes are those with two electrode wires located inside the cannula of a hypodermic needle, where only their tips are active. Dedo (25) stated that, in order to avoid interfering signals from adjacent muscles, a bipolar Journal of Voice, Vol. 6, No. 2, 1992

needle electrode is preferable to a " m o n o w i r e " concentric needle electrode. Because the amplitude of the recorded signal depends on the spectrum of the recorded potentials together with the distance between the electrodes, the amplitude recorded by the bipolar needle will be much smaller than that recorded by a unipolar needle. Due to the differentiating action of the bipolar electrode, although desirable, it is difficult to compare recordings obtained using one electrode with those obtained using other types of electrodes (24). A multielectrode is a relatively large electrode with several pick-up active areas on the shaft. Electrical potential can be recorded between any of these closely spaced active electrode spots. This electrode has no place in laryngeal EMG. Hooked-wire electrodes have been extensively described by Basmajian and Stecko (26) and by Hirano and Ohala (27). Hooked-wire electrodes have several advantages over needle electrodes due to their flexibility and lightness: they are not easily displaced because they are anchored by hooks; they do not interfere with phonation or speech; and they permit more localization of the area from which electrical activity is recorded (28). Two thin isolated wires with bare ends are threaded through a thin hypodermic cannula, and cut 0.5-1 mm away from the tip of the cannula. The opposite ends of the insulation are abraded for connection to the differential amplifier. The hooked wire electrodes are inserted into the muscle with the hypodermic needle, which is later removed, leaving the wire in place. The main disadvantage is the unfixed distance between the flexible wire electrode tips in every insertion: this affects reliable comparison of the results, due to the changing parameters of the MUAPs. Although electrodes may be custom-made, several manufactures are supplying highly standardized, ready-made electrodes of different sizes and types. Using off-the-shelf electrodes is more expensive but less costly in time.

Preamplifiers and differential amplifiers The amplifier system must satisfy the following requirements (29): (a) high-frequency uniform voltage gain over the whole frequency range; (b) frequency range of 2-20.000 Hz, to suit laryngeal electromyographic recordings, in which frequency changes of 100 p~V may occur in <1 ms; (c) differential input, to reject voltages of in-phase signals that are identical, both in amplitude and time, at its

ELECTROMYOGRAPHY AND NEUROGRAPHY two input terminals, which would normally interfere with the recorded muscle potentials. A rectifying unit A rectifying unit is an optional addition and is used to change the raw EMG into an overall integrated EMG (i.e., muscle activity curve, with amplitude versus time) (30,31).

5. 6. 7. 8.

Monitoring system An oscilloscope with dual or multiple channels preferably supplemented with a storage facility is essential for monitoring signals during the experiment. An audio system with a loud-speaker is an important monitoring option. Through this audio system the clinician may observe the MUAPs and other signals and may distinguish between remote (muffled) MUAPs and near sharp MUAPs picked up by the electrode. This can be of assistance in fine adjustment of electrode placement. Write-out systems There are many types of write-out systems: photographic film systems (32), heat-sensitive recording paper systems, FM recording systems, and computer systems. In laryngeal electromyographies, there is great need for write-out systems of high-frequency response, because spiky potentials of high rise time may be recorded. Many investigators use custom-made apparatus for recording laryngeal EMG activities, essentially made of an electrode input socket, plugged into a preamplifier and differential amplifier, together with an optional rectifying unit attached to a mimeograph with jet-ink paper write-out system of a linear frequency response up to 700 Hz (33). However, there are manufacturers that produce feasible and reliable ready-made apparatus that offer the options needed for clinical electromyography and neurography. The new computerized systems offer programs for on-line monitoring as well as subsequent analysis.

9. 10. 11. 12. 13. 14.

15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25.

REFERENCES 1. Weddell G, Feinstein B, Pattle RE. The electrical activity of voluntary muscle in man under normal and pathological conditions. Brain 1944;67:178-257. 2. Feinstein B. The applications of electromyography to affections of the facial and the intrinsic laryngeal muscles. Proc R Soc Med 1945;39:817--8. 3. Macbeth RG. Proc R Soc Med 1946;39:819. 4. Kotby MN. Percutaneous laryngeal electromyography.

26. 27. 28. 29. 30.

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Standardization of the technique. Folia Phoniatr 1975;27: 116-27. Katsuki Y. The function of the phonatory muscle. Jpn J Physiol 1950;1:29-36. Portmann G, Humbert R, Robin JL, Laget P, Husson R, Monnler AM. Etude electromyographie des cordes vocales chez l'homme. C R Soc Biol (Paris) 1955;149:296-300. Spoor A, VanDisheck HAE. Electromyography of the human vocal cords and the theory of Husson. Practica Otorhinolaryngol 1958;20:253-360. Greiner GF, Iseh F, Isch-Treussard C, Ebtinger-Jouffroy J, Klotz G, Champy M. L'electromyographie appliquee a la pathologie du larynx. Acta Otolaryngol 1960;51:319-31. Kotby MN. Haugen. Clinical application of electromyography in vocal fold mobility disorders. Acta Otolaryngol 1970b;70:428-37. Shipp T, Fishman BV, Morrissey P, McGlone R. Method and control of laryngeal EMG electrode placement in man. J Acoust Soc Am 1970;48:429-30. Faaborg-Andersen K. Electromyographic investigation of intrinsic laryngeal muscles in humans. Acta Physiol Scand [Suppl] 1957 ;41:140. Guerrier Y, Basseres F. Electromyographic pharyngolaryngee. Presentation d'appareiiage. Ann Otolaryngol (Paris) 1965;82:589-94. Hirose H. Electromyography of the articulatory muscles. Current instrumentation and technique. Status report on speech research, Haskins Laboratory Sr-25 1971:73-86. Kittel G, Thurmer St. Thumfart W. Das Kelkopf-EMG als phoniatrische Untersuchungs methode fur prognose und verlaufskontrolle von stimmlippen Lahmungen. Sprache S timme Gehor 1982;6:114-7. Thumfart WF. In: Samii M, Janetta PJ, eds. Endoscopic electromyography and neurography in "the cranial nerves." Berlin: Springer Verlag, 1981:597--606. Thumfart F. From larynx to vocal ability new electrophysiological data. Acta Otolaryngol (Stockh) 1988;105:425-31. Von Stuckrad H, Lakatos T. Uber ein neues Lupenendoskop (pharyngoscop). Laryngol Rhinol Otol 1975;54:33640. Fink BR, Basch M, Epanchin V. The mechanism of opening of the human larynx. Laryngoscope 1956;66:410-25. Kotby MN. Electromyography of the laryngeal muscles. [Thesis]. Cairo, Egypt: Ain Shams University, 1967. Stempel J, Weiler E, Whitehead W, Komray R. Electromyographic biofeedback training with patients exhibiting a hyperfunctional voice disorder. Laryngoscope 1980;90:471-6. Dedo HH, Ogura JH. Vocal cord electromyography in the dog. Laryngoscope 1965;75:201. Dedo HH, Dunker E. Volume conduction of motor unit potentials. Electroencephalogr Clin Neurophysiol 1966;20: 608-13. Dedo HH, Hall WN. Electrodes in laryngeal electromyography. Ann Otolaryngol Rhinol Laryngol 1969;78:172-80. Pollak B. The waveshape of action potentials recorded with different types of electromyographic needles. Med Biol Eng Comput 1971 ;9:657--64. Dedo HH. The paralyzed larynx: an electromyographic study in dogs and humans. Laryngoscope 1970;80:1455-519. Basmajian JV, Stecko G. A new bipolar electrode for electromyography. J Appl Physiol 1962;17:849. Hirano M, Ohala J. Use of hooked-wire electrodes for electromyography of the intrinsic laryngeal muscles. J Speech Hear Res 1969;12:362-73. Hirano M. Clinical examination of voice. New York: Springer-Verlag, 1981. Dejonckere PH. E.M.G. of the larynx. M. Pietteur, Louvain, Belgium: University of Louvain, 1987. Kewley-Port D. Computer processing of E.M.G. signals of Journal of Voice, Vol. 6, No. 2, 1992

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Haskins Laboratories. H a s k i n s Laboratories status report on speech research. Sr-33 1973;173-83. 31. Hirose H. Posterior cricothyroid as a speech muscle. A n n Otol 1976;85:334-42. 32. Terence DR, Sasaki C. A technique for electromyographic evaluation of intrinsic laryngeal muscle activity in man. Laryngoscope 1981 ;91:1191-3. 33. Fritzell B, Kotby MN. Observations on thyroarytenoid and palatal levator activation for speech. Folia Phoniatr 1976; 28:1-7.

Section V. Kinesiological Electromyography in Laryngeal and Voice P h y s i o l o g y a n d Speech Sciences

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Methodology As discussed in the previous section, hookedwire electrodes have some advantage over other electrodes, and for experimental purposes are the electrodes of choice. The electrical signals are fed into a custom-made EMG preamplifier and a differential amplifier in the form of plug-in units that can be used with a mimeograph that offers a jet-ink paper write-out system. This armamentarium gives maximum flexibility in achieving the objectives of the study. The rectifying units are used to provide an impression of the overall muscle activity.

Results Basic function of the larynx At rest. A background tonic or postural activity is usually present in the electromyographic recordings of the intrinsic laryngeal muscles during rest "quiet breathing" (1-5). Wyke (6) suggested that the basic tonic activity of the intrinsic laryngeal muscles was determined by the reflexogenic afferent discharges generated from the low-threshold mechanoreceptors located within each muscle. The continuous slight stretch of the muscle's fibers between its attachments causes the continuous excitation of these mechanoreceptors. Deep breathing. The cyclic variations in laryngeal intrinsic muscle activity during quiet breathing are negligible and only become apparent in deep respiration (Fig. 8). Several authors agree that this resting laryngeal electrical activity increases in frequency and amplitude during inspiration only (1,2,3,7). Others postulate that there is increased Journal of Voice, Vol. 6, No. 2, 1992

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activity in the adductors of the vocal folds during expiration, which relax during inspiration (8). Kotby and Haugen (9) found an increase in activ= ity of both abductors and adductors with forced inspiration. This increased activity was interpreted to be a mechanism to stabilize the cricoarytenoid joint and stiffen the edges of the folds. In so doing the mechanism prevents the folds from flapping and collapsing in front of the incoming jet of air during inspiration. Knutsson et al. (10) and Haglund (5) found that the discharge frequency in some motor units was independent of the respiratory phase, while in other motor units it varied with the different respiratory phases: some were found to discharge only in the respiratory phase; others were found to discharge continuously with modulation according to the respiratory phase. Studies by Wyke (6) indicated that the magnitude of respiratory oscillations of the motor unit activity in the laryngeal muscles is related to the degree of background tonic postural activity prevailing in the muscles. The activity of the sternothyroid muscle, a member of the extrinsic laryngeal group, was investigated during respiration and was found to exhibit a pronounced electrical activity during inspiration (3,4,11). The muscle was assumed to have an influence on widening the glottis, thus indicating the in-

ELECTR OM Y O G R A P H Y A N D N E U R O G R A P H Y

175

FIG. 8. Respiratory fluctuations with deep breathing. I n c r e a s e d activity during inspiration in all the internal muscles of the larynx (abductors and adductors).

fluence of the extrinsic laryngeal muscles on glottic size and configuration. Sphincteric actions. Faaborg-Anders on (1), Kotby (3), Hirano and Ohala (12), Haglund (5), and Fink (13) stated that during coughing and swallowing there was a considerable increase in the EMG potentials in all the adductors just before the onset of an audible sound (Fig. 10). Coughing and swallowing were found to be associated with a special shift of baseline, most probably due to electrode movement (4). The same authors recorded the activity of the posticus muscle in glottal sphincteric actions as coughing, swallowing, and straining. They suggested that the posticus activity was the balancing force needed to counteract any excessive forward pull produced by the lateral cricoarytenoid and possibly the thyroarytenoid and cricothyroid muscles on the arytenoid cartilage (14). On the other hand, Sasaki et al. (15) found an abrupt inhibition of the action potentials of the posticus muscle just before the sphincteric actions.

Phonation. As a general rule, the electrical activity of the laryngeal muscles is markedly increased during phonation. This increase in activity begins and reaches its maximum before an audible tone is recorded by the pick-up microphone (1,3,6,16) (Fig. 11). This latent time is not only the time needed for the propagation of the sound between the source (vocal folds) and the pick-up microphone in front of the lips, it may also be explained by a prephonatory muscle tuning in order to adjust the vocal folds for the production of a particular sound (pitch and intensity). Fritzell and Kotby (17), in their study to compare the activity of the thyroarytenoid and levator muscles, confirmed the presence of the latent time and found it to be longer when the initial sound was voiced (300 ms) than when it was unvoiced (100 ms). The thyroarytenoid was also found to have a longer latency time than for the levator palati muscle. The authors suggested that the latent time .

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was a prephonatory laryngeal activity related to the type of laryngeal adjustment (voicing and devoicing). Their results were in agreement with FaaborgAndersen (1), who called this period the prephonatory tuning and found it to be largest for vowel syllables and smaller for nasals, voice consonants, and voiceless consonants in decreasing order. Style ofphonation. In their EMG investigation of some laryngeal muscles in relation to the style of phonation, Hirano et al. (18) suggested that the vocalis muscle was the most important muscle in regulating the style of phonation: activity was found to be greatest for the hypertensive style; moderate for the optimum style; smallest for the hypotensive style, The sternohyoid muscle was also found to assist in regulating the style of phonation. They concluded that at the level of the glottis, the variation of the style of phonation was mainly attributed to changes in the glottal resistance. Register control. The EMG patterns of the laryngeal muscles were studied by many authors during phonation of sustained tones in different registers (19-21). Faaborg-Andersen (1) reported that the vocalis muscle was active in chest voice and less active in falsetto voice. Hirano (22) confirmed the fact that the heavier the register, the greater the vocalis muscle activity became. The lateral cricoarytenoid tended to be more active for heavier registers but not as the vocalis (22). He also found register shifts to be accompanied with marked changes in the vocalis activity. Whereas register shifts from heavy to light were associated with a decrease in vocalis activity, shifts from light to heavy were associated with increase in vocalis activity. Pitch control: modal register. Vennard et al. (23), in their laryngeal EMG studies, found that the cricothyroid was the primary pitch agent in the Journal of Voice, Vol. 6, No. 2, 1992

chest register. Each degree of rise in the musical scale was corresponded by an increase in the activity of the muscle. Studies by Hirano (22) have shown that in the modal register the activity of the cricothyroid, lateral cricoarytenoid, and vocalis were always positively related to the fundamental frequency, with the cricothyroid muscle playing the most important role. Pitch control: falsetto register. Vennard et al. (23) reported that in light registration, or falsetto, the breath was the primary pitch agent. The laryngeal muscles showed great independence and did not parallel each other as in chest register. This was confirmed by Hirano (22), who found that the activity of the cricothyroid, lateral cricoarytenoid, and vocalis muscles were not always positively related to Fo in falsetto. Intensity control: chest register. Katsuki (24), one of the pioneers in the study of laryngeal activity in different tones using EMG, reported that in loud tones the vocalis muscle was active, and in soft tones it was respectively passive. On the other hand, Faaborg-Andersen (1) found no significant increase in the electrical activity of the vocalis muscle with increasing intensity of phonation. Afterwards, several authors observed participation of the vocalis in regulating the intensity of voice, especially in chest register (18,19,21). Hirano (22) stated that the activity of the vocalis changes markedly in proportion to vocal intensity in the modal register. The activity of the lateral cricoarytenoid and interarytenoid muscles were also found to increase with increased vocal intensity, but less consistently than in the case of the vocalis muscle. Intensity control: falsetto register. Hirano (22) found that in falsetto register none of the laryngeal muscles showed evidence of a significant contribution to intensity control. He suggested that the vocal intensity in falsetto register was almost exclusively regulated by the expiratory air pressure. Laryngeal adjustments in singing. EMG studies on the contribution of the laryngeal muscles in the regulation of important parameters during singing were completed by Vennard, Hirano, Ohala, and Fritzell (21-23,25). They concluded that the cricothyroid muscle activity is responsible for regulation of vocal register and fundamental frequency, whereas the vocalis muscle activity was responsible for regulating vocal register and intensity. The activity of both the lateral cricoarytenoid and the interarytenoid was found to contribute to the vocal

ELECTROMYOGRAPHY AND NEUROGRAPHY register, fundamental frequency, and intensity, but to a lesser extent. The posticus muscle activity was found to be responsible for vocal fold abduction with no specific contribution to the voice control in singing (22). Dejonckere (26) investigated the activity of the laryngeal muscles during silent singing and found that they exhibited the same activity patterns as in normal singing but with smaller electrical activity and less clear-cut transitions. Whisper. An increase in the electric activity of the vocalis muscle in case of whispered voice was recorded by several authors (1,13,27-29). The activity, although present, was less than observed during normal phonation.

Speech sciences The use of laryngeal EMG in speech studies in different languages provides great insight into the different laryngeal adjustments made during the speech act. Laryngeal adjustments in silent speech. Several investigators have observed an increase in the vocalis activity with silent reading, especially when the subject was requested to read an unfamiliar text in a foreign language (13,29). Moreover, Fritzell and Kotby (17) recorded an increase in the vocalis muscle activity in subjects while listening to the investigators provide oral instructions. Moses (30) labeled this phenomenon "creative hearing." Laryngeal adjustment for different speech sounds. The basic laryngeal mechanisms are considered to comprise three different postures of the larynx: those of breathing, phonation, and airway protection. Sawashima and Hirose (31) stated that these postures are also used in the production of speech sounds of different languages, as glottal adductionabduction gestures or the glottal stop gesture. Several studies on the laryngeal articulatory gestures by authors such as Hirose and Gay (38), Hirose and Ushijima (33), and Hirose et al. (43) demonstrated that the principal mechanism underlying the abduction-adduction of the glottis is the reciprocal activation of the abductor-adductor groups of the larynx. The larynx is geared to speech mode (adduction during voicing) by activation of all the laryngeal adductors and suppression of the posticus (abductory); the finer adjustments of the glottal aperture for the various speech sounds are provided by the interarytenoid with supportive action of the lateral cricoarytenoid (32). Hirose (37) found the posticus activity to be of

177

particular importance in the production of voiceless obstruents. Activity increased for the production of the voiceless portion of the test words and suppressed for their voiced portion, while the interarytenoid showed a reciprocal pattern. This was found to be true for several different languages including Swedish (37), American English (38), Icelandic (39,40), and Japanese (33). Similarly, Yoshioka et al. (41) demonstrated that voiceless fricatives (e.g.,/s/) tend to require a wide glottal opening gesture when compared with the unaspirated stops (e.g.,/p/), and that the peak timing of the glottal opening for the voiceless fricatives is considerably earlier than that for the voiceless stops. They also found the glottal movement for the production of obstruent clusters to depend on the timing of the oral release for the first obstruent. Accordingly, the peak activity of the posticus muscle for /sp/, which is attained during the friction noise for/s/, is earlier than that for/ps/, in which the peak activity of the posticus muscle approximately coincides with the peak activity for the oral release of the stop/p/. Further studies by Yoshioka et al. (38,42) proved that a voiceless obstruent specified with aspiration or friction noise tends to require a separate opening gesture, caused by activity of the posticus, whereas an unaspirated stop in a voiceless environment can be produced within the opening gesture attributed to an adjacent aspirated stop or fricative. Thus, the /sk # sk/sequence in English is produced with two separate opening gestures and two peak activities of the posticus, whereas a / s k s # k/sequence is produced with three opening gestures and three peak activities of the posticus. Intrinsic laryngeal muscles other than the posticus and interarytenoid were also found to contribute to voicing/devoicing distinctions. Hirose (43) found the activity of the vocalis and lateral cricoarytenoid to be less markedly suppressed for voiceless consonants. Dixit (35) suggested that the cricothyroid activity was related to devoicing especially in word-initial positions; yet studies by Sawashima and Hirose (31) did not confirm any cricothyroid contribution to voicelessness. Laryngeal and articulatory muscle coordination in speech. The EMG study of Fritzell and Kotby (17) on the laryngeal and palatal activity during speech showed that the thyroarytenoid (vocalis) was not an articulatory muscle. It became active with the start of speech and maintained that activity for the Journal of Voice, Vol. 6, No. 2, 1992

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M. N. K O T B Y E T A L .

duration of the speech sample. On the other hand, the levator muscle, which showed on and off activity specific to the sound being articulated, was considered a true articulatory muscle. Thyroarytenoid activity preceded the onset of the speech act and maintained activity throughout speech except for sentences beginning with voiceless sounds, where it was diminished. The duration of this devoicing period varied between 50 and 100 ms. Laryngeal adjustments for word tones and accents. Several EMG studies were conducted to clarify the role of the intrinsic laryngeal muscles in accents. Simado and Hirose (44) and Yoshoka et al. (42), in their study on the Japanese language, found that the activity of the vocalis and cricothyroid muscles peaked for the accent kernel. The peak value of the vocalis was much higher for the accented first mora than for the accented second mora. The cricothyroid did not demonstrate such noticeable differences. In the intervocalic position, EMG activity of both the vocalis and cricothyroid correlates directly with accent regardless if a voiced or voiceless fricative is being produced. Similar studies were conducted for the Swedish accented language by Garding et al. (37). They recorded greater activity for the vocalis muscle in the grave prosodic accented words compared with its activity in the acute prosodic accented words. The cricothyroid muscle showed a clear and consistent correlation with the fundamental frequency curve.

REFERENCES 1. Faaborg-Andersen K. Electromyographic investigation of intrinsic laryngeal muscles in humans. Acta Physiol Scand [Suppl] t 957 ;41:140. 2. Buchtal F. An introduction to electromyography. Copenhagen: Munksgaard, 1957. 3. Kotby MN. Electromyography of the laryngeal muscles. [Thesis]. Cairo, Egypt: Ain Shams University, 1967. 4. Kotby MN, Haugen LK. The mechanics of laryngeal functions. Acta Otolaryngol 1970;70:203-11. 5. Haglund S. Electromyography in the diagnosis o f laryngeal motor disorders. Stockholm: Boktrycker:Ab Thule, 1973. 6. Wyke B. Ventilatory and phonatory control systems. London: Oxford Press, 1974. 7. Weddell G, Feinstein B, Pattie RE. The electrical activity of voluntary muscle in man under normal and pathological conditions. Brain 1944;67:178-257. 8. Buchtal F, Faaborg-Andersen K. Electromyography of laryngeal and respiratory muscles. Ann Otol Rhinol Latyngol 1964;73:118-23. 9. Kotby MN, Haugen LK. Critical evaluation of the action of the P.C.A., utilizing direct EMG study. Acta Otolaryngol 1979b;70:260-8. Journal of Voice, Vol. 6, No. 2, 1992

10. Knutsson E, Martenson A, Martensson B. The normal electromyogram in human vocal muscles. Acta Otolaryngol 1969;68:526--36. 11. Fink BR, Basck M, Epandchir V. The mechanisms of opening the human larynx. Laryngoscope 1956;66:410--25. 12. Hirano M, Ohala J, Vennard W. The function of the laryngeal muscles in regulating fundamental frequency and intensity of phonation. J Speech Hear Res 1969b;12:616-28. 13. Fink BR. The human larynx. A functional study. New York: Raven, 1975. 14. Kotby MN, Haugen LK. Critical evaluation of the action of the P.C.A., utilizing direct EMG study. Acta Otolaryngol (Stockh) 1970;70:260-8. 15. Sasaki CT, Fukuda H, Kirchner JA. Laryngeal abductor activity in response to varying ventillatory resistance. Jr A m Acad Opthalmol Otolaryngol 1973;77:403-10. 16. Dejonckere PH. E.M.G. o f the larynx. Louvain, Belgium: University of Louvaln, 1987. 17. Fritzell B, Kotby MN. Observation on thyroarytenoid and palatal levator activation for speech. Folia Phoniatr 1976; 28:1-7. 18. Hirano M, Koike K, Joyner J. Style of phonation. Arch Otolaryngol Head Neck Surg 1969;89:902-7. 19. Fink BR. Adaptation for phonatory efficiency in the human vocal folds. Ann Otolaryngol Rhinol Laryngol 1962;71:7985. 20. Hirano M, Ohala J, Vennard W. The function of the laryngeal muscles in regulating fundamental frequency and intensity of phonation. J Speech Hear Res 1969;12:616-28. 21. Vennard W, Hirano M, FritzeU B. The extrinsic laryngeal muscles. N A T S Bull May-June 1971:27. 22. Hirano M. Vocal mechanisms in singing: laryngological and phoniatric aspects. J Voice 1988;2:51-69. 23. Vennard W, Hirano M, Ohala J. Chest head and falsetto. NATS Bull December 1970:27. 24. Katsuki Y. The function of the phonatory muscles. Jpn J Physiol 1950;7:29-36. 25. Vennard W, Hirano M, Ohala J. Laryngeal synergy in singing. ]VATS Bull October 1970:27. 26. Dejonckere PH. Some electromyographic data about auditire and proprioceptive mechanisms for pitch control in singing. In: Waar-Garrat, Waar. Proceedings o f the 2nd Conference o f lDRS 1982:43-51. 27. Greiner GF, Isch F, Treussard C, Ebtinger-Jouffroy J, Klotz G, Champy M. L'electromyographie appliquee a la pathologie du larynx. Acta Otolaryngol 1960;51:319-31. 28. Buchtal F, Faaborg-Andersen K. Electromyography of laryngeal and respiratory muscles. Ann Otolaryngol Rhinol Laryngol 1964;73:118-23. 29. Shipp T, Fischman BV, Morrissey P, MacGlone RE. Method of control of laryngeal EMG electrode placement in man. J Acoust Soc Am 1970;43:429-30. 30. Moses PJ. The voice o f neurosis. New York: Grune & Stratton, 1954:11. 31. Swashima M, Hirose H. Laryngeal gestures in speech production. Ann Bull 1980;14:29-51. 32. Hirose H, Gay T. The activity of the intrinsic laryngeal muscles in voicing control. An electromyographic study. Phonetica 1972;25:140--64. 33. Hirose H, Ushijma T. Laryngeal control for voicing distinction in Japanese consonant production. Phonetica 1978;35: 1-10. 34. Hirose H, Yoshioka H, Niimi S. A cross language study of laryngeal adjustments in consonant production. Ann Bull RILP 1978;12:61-71. 35. Dixit RP. Neuromuscular aspect of laryngeal control. Ph.D. dissertation, University of Texas at Austin.

ELECTROMYOGRAPHY AND NEUROGRAPHY 36. Hirose H. Posterior cricoarytenoid as a speech muscle. Ann Otolaryngol 1976;85:334--42. 37. Garding E, Fujinura O, Hirose H. Laryngeal control of Swedish word tones. Research institute o f logopedics and phoniatrics. Annual bulletin No. 4, University of Tokyo, Japan, 1970. 38. Yoshioka H, Lofqvist A, Hirose H. Laryngeal adjustments in the production of consonant clusters and geminates in American English. Haskins Laboratories Status Report on Speech Research, SR-59/60, 1979:120-51. 39. Lofqvist A, Yoshiioka H. Laryngeal activity in Icelandic obstruent clusters. J Acoust Soc Am 1980;68:792-801. 40. Lofqvist A, Yoshioka H. Laryngeal activity in Iceland obstruent production. Nordic J Linguistics 1981;4:1- 18. 41. Yoshioka H, Lofqvist A, Collier R. Laryngeal adjustments in Dutch voiceless obstruent production. Ann Bull ILP Tokyo 1982b;16:27-35. 42. Yoshioka H, Lofqvist A, Hirose H. Laryngeal voiceless sound production. J Phoniatr 1982a;10:1-10. 43. Hirose H. Laryngeal adjustments in consonant production. Phonetica 1977;34:289-94. 44. Simado Z, Hirose H. The function of the laryngeal muscles in respect to the word accent distinction. University of Tokyo, Japan. Ann Bull Logopedics and Phoniatrics 1970;4.

Section VI. Clinical Applications of E l e c t r o m y o g r a p h y a n d N e u r o g r a p h y in Laryngeal Disorders ELECTROMYOGRAPHY Despite the value of EMG in studying the action of muscles in vivo (kinesiology), it is also an important tool for the diagnosis of neuromuscular pathologies. Accordingly and for technical purposes, laryngeal EMG may be classified into two main categories: (a) procedures for kinesiological studies and (b) procedures for clinical evaluation of laryngeal neuromuscular pathology. INDICATIONS Any neuromuscular pathology in the larynx may show itself mainly as a mobility disorder of one or both vocal folds. The nature and degree of this mobility disorder is difficult to assess by the clinical mirror or other visual examination tools only. In these diseases, the degree and extent of the residual movements may vary considerably in similar etiological categories. At the same time, the position of the immobile vocal fold cannot convey the type and extent of the paresis. Faced with these diagnostic problems, it was felt by several investigators (1-8) that there is a necessity for applying electromyography as a clinical diagnostic aid to show the neuromuscular status of the various laryngeal muscles in cases of vocal fold mobility disorders.

179

DIAGNOSIS Etiological disorders The EMG investigation of the laryngeal muscles can help in differentiation of mechanical and functional factors from neuromuscular lesions producing vocal fold mobility disorders. It can also differentiate between neurogenic and myogenic lesions (5,6,8,9).

System affected The EMG investigation can diagnose the nervemuscle system affected, whether the inferior laryngeal system, the superior laryngeal system, or both (4-8,10-12).

PROGNOSIS Monitoring spontaneous recovery EMG studies can detect early stages of recovery of partial laryngeal nerve lesion far before clinical detection of return of movement in the immobile vocal fold. The increase in the number of the motor unit action potentials with an increasing percentage of polyphasic potentials denotes early muscle reinnervation (5-8,10). On the other hand, Satoh et al (13) and Hiroto (14) found it insufficient to rely on the electric activity (or MUAPs) recorded from apparently antagonistic groups of vocal fold muscles in monitoring laryngeal innervation without observation of the active gross (abduction-adduction) movements of the vocal folds. Monitoring results of surgical reinnervation Bilateral injury of the recurrent laryngeal nerves is an unfortunate but not an uncommon complication of thyroid surgery. Several attempts were made to obtain reinnervation of the posticus muscle (the vocal fold abductor) to relieve the respiratory stridor common among patients. The reinnervation attempts fall into the following three main categories. Recurrent nerve suturing (self-reinnervation)

Such experimental operations were begun in 1927 by Colledge and Balance (15). They were also tried by several other authors but the results were never satisfactory concerning the return of gross (abduction-adduction) movements (16-18). Better results were obtained by cutting the adductor branch of the recurrent laryngeal nerve after neuroraphy of the nerve (19,20). Journal of Voice, Vol. 6, No. 2, 1992

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M. N. K O T B Y E T AL.

Ansa hypoglossi nerve anastomosis (including nerve-muscle pedicle graft)

The concept of this technique lies in the implantation of the functioning motor endplates of the sternohyoid muscle in canines (21-23) or the omohyoid muscle in humans (24) together with the ansahypoglossi into the posterior cricoarytenoid muscle. Yet the results of these operations were found to be uncertain, with no solid evidence of reinnervation of the posticus via the nerve in the pedicle (25,26).

Thus, although it was thought that laryngeal EMG could detect early reinnervation in the paralyzed laryngeal muscle, it was found unsatisfactory, because the return of electrical activity in a muscle and its effective shortening (contraction) do not necessarily follow each other closely. Agonistic muscle may contract at the same time as its antagonistic muscle because the activating nerve fibers to both m u s c l e s belong to one s y s t e m (18,29,34,35).

Phrenic nerve anastomosis

Phrenic nerve/recurrent nerve anastomosis. Clinical experiments on recurrent nerve/phrenic nerve anastomosis were begun in 1924 by Ballance (27). During the following years, several authors, using a similar technique, reported more or less favorable results (25,28,29). Phrenic nerve implantation into the posticus muscle. Fex (30) stated that reinnervation should be a selected one, restricted to the posticus muscle. He implanted the phrenic nerve directly into the posticus muscle (in cats). Later, Taggart (31) and Morledge et al. (32) used a similar experimental design in dogs. Crumley (33) used a similar technique in humans. Brondbo et al. (34) compared the three different techniques of experimental posticus muscle reinnervation and suggested that the phrenic nerve/ recurrent nerve anastomosis technique would be the best alternative if reinnervation of the posticus muscle in paralyzed larynges was attempted. They evaluated their results by documentary photos of the vocal fold excursions (during quiet respiration and forced respiration, and by electrical stimulation of the anastomosed recurrent laryngeal nerve), rather than recording the EMG pattern of the reinnervated posticus muscle (which was used in earlier studies).

STUDY OF SOME SPECIAL PHENOMENA

Spastic dysphonia Great interest in the laryngeal EMG of patients with spastic dysphonia was started after Dedo (36) described the section of the recurrent nerve as a treatment for the condition. Blitzer et al. (37) demonstrated through their clinical observation and EMG data on such patients that spastic dysphonia was not a spastic disease. In their study, they identified patients with tremors, myoclonus, and pyramidal and extrapyramidal diseases among spastic dysphonic patients. The remainder of the patients had clinical and EMG findings consistent with dystonia. Thus, they classified spastic dysphonia as a type of dystonia that may present focally or in association with other dystonic movements. Thumfart (8) in his studies on spastic dysphonics found typical noticeable discoordination in the EMG of the vocal muscles together with a pre- and postphonatoric prolonged activity of the inner laryngeal muscles. The authors found the EMG patterns of patients suffering from spastic dysphonia to be much like the EMG patterns of their coughing (Fig. 12). They assumed that in spastic dysphonia, the higher function of purposive phonation is changed into a primitive reflexive sphincteric action.

FIG. 12. Spasmodic dysphonia. Phonatory activity with attempted sustained vowel comes in short bursts similar to coughing activity.

Journal of Voice, Vol. 6, No. 2, 1992

ELECTROMYOGRAPHY AND NEUROGRAPHY

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of stuttering. Thurmer et al. (39) found prephonatory hyperactivity in the EMG of the phonatory and articulatory muscles of some stutterers, and prearticulatory hyperactivity in the articulatory muscles of other stutterers with continuous activity in the vocal muscles. He also found stutterers with EMG patterns combining both previous characteristics.

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For standard clinical purposes, the percutaneous approach proved to be the most suitable in the hands of many investigators (3,5,6,40--43).

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Set-up This can take place in the out-patient clinic with the patient lying in the recumbent position and the neck slightly extended. Shielding of the room is not necessary with modern apparatus, but the room should be quiet.

FIG. 13. Normal laryngeal M U A P s in a case of sulcus glottideus.

Sulcus glottideus Cases of sulcus glottideus show apparent atrophy of the vocal folds with variable degrees of glottal waste. Kotby (38) found the electrical activity of the thyroarytenoid muscle in cases of sulcus vocalis to be normal, pointing to the fact that sulcus glottideus is probably a mucosal defect with no muscular affection, despite the commonly observed phonatory glottic waste (Figs. 13, 14, 15).

Stuttering EMG studies can give an objective clue to the participation of the laryngeal muscles in the tonic repetitions or blocks occurring in the phonatory system of the larynx in association with the moment

Preparation The patient. Little or even no preparation may be needed for the patient using the percutaneous approach. Hirano and Ohala (41) used topical anesthesia for surface anesthesia of the laryngeal mucosa, especially when recordings were obtained from the vocalis and interarytenoid muscles. Haglund (6) injected 0.25 mg atropine subcutaneously about 15 min before the examination in order to reduce secretions and diminish irritation and coughing. On the other hand, Kotby and Haugen (5) used no patient preparation for their percutaneous technique, because all electrode maneuvers were performed submucosally. Grounding in laryngeal EMG could be done by placing a ground lead on the patient's ear lobe (44), by placing a chest electrode between the heart and larynx and connecting the subject to the ground (6), or by using a wrist bracelet indifferent electrode (45).

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Journal of Voice, Vol. 6, No. 2, 1992

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The concentric needle electrodes are the most commonly used electrodes for clinical purposes (5,6,44). Dedo and Hall (46) thought that the bipolar concentric needle electrodes were the only reliable electrodes capable of recording potentials from each intrinsic laryngeal muscle separately. They found the pick-up distance of the unipolar concentric needle electrodes to be >0.5 cm, whereas the bipolar concentric needle electrodes reliably recorded potentials only from the muscle into which they were inserted. On the other hand, Kotby and Haugen (5) proved that with concentric needle electrodes (DISA 13 K 51) no "cross-talk" recordings of MUAPs were encountered across the intrinsic laryngeal muscles. For clinical laryngeal EMG, ready-made commercial standard EMG apparatus are satisfactory (e.g., Alvar, Dantec, Nihon Kohden).

To reduce the problem of electrode displacement, which can be encountered with needle electrodes, a new electrode with a hook can be used (Fig. 19). Protocol

Muscles investigated. The thyroarytenoid and the cricothyroid muscles on each side are investigated, as a representative of the inferior and superior laryngeal nerve-muscle systems. The posticus muscle is also preferably studied because it represents the "antagonist" to the first two muscles, although not routinely, because it is difficult to approach. Kotby and Haugen (5) suggested that the first sitting of laryngeal EMG should include recordings from the posticus muscle. Activities recorded. EMG recordings from the laryngeal muscles are obtained at rest (during quiet breathing), during deep breathing, and during phonation at comfortable pitch and loudness levels. EMG recordings also are obtained with different sphincteric functions of the larynx (straining, coughing, and swallowing). The latter recordings are usually done last to avoid displacement of the laryngeal electrodes. Adjustments

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FIG. 16. Spontaneous fibrillation potential in a severe neurogenic lesion of a laryngeal muscle. Journal of Voice, Vol. 6, No. 2, 1992

Proper electrode placement can be monitored by listening through the loud speaker to the sharp MUAPs and observing through the oscilloscope screen. Registration of the MUAPs in the best suitable morphological proportions can be achieved by variations in the oscilloscope gain. Illustration of the overall muscle activity as well as the individual MUAPs can be done by changing the sweep velocity of the recording system, thus allowing the demonstration of the various parameters of the individual MUAP. Specially equipped EMG apparatus (e.g., Alvar, Dantec, Nihon Kohden) can measure the different parameters of the individual MUAP on the screen. COMPLICATIONS Occasionally, percutaneous laryngeal EMG may be complicated by puncturing of the cricothyroid

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venous arcade. Bleeding is checked by digital compression for a few minutes. A small subcutaneous hematoma may accumulate for a day or two and disappear spontaneously thereafter. Laryngeal spasm may also occur if the needle electrodes accidentally penetrate the unanesthetized laryngeal mucosa. In this event the test may need to be postponed until the patient regains "laryngeal ease." Vocal fold edema is another complication that may be encountered using laryngeal electrodes via the percutaneous route (5,7). INTERPRETATION At rest Under normal conditions, a properly relaxed skeletal muscle is electrically silent. In cases of neurogenic disturbances, the affected muscle may show at rest various types of spontaneous electrical activity. These may be in the form of brief (0.5-3 ms) biphasic potentials of a very small amplitude (50--200 txV), designated as fibrillation potentials (Fig. 16), or in the form of monophasic positive potentials known as the positive denervation potentials (2-7,45). The small internal laryngeal muscles can never reach the state of rest with electrical silence. Quiet breathing is the maximum status of rest that the laryngeal muscles can approach. There is always a certain degree of continuous resting tonic activity, in the form of a low-frequency discharge of MUAPs of brief duration and low amplitude (5). That is, the

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identification of the spontaneous muscle activity encountered in cases of neurogenic lesions would be difficult using laryngeal EMG because of the constant background postural activity. Similarly, the insertion activity would also be lost in the background of continuous laryngeal activity. Interference pattern In laryngeal movements, unlike peripheral skeletal muscles, there is little chance for gradation of the degree of contraction. Accordingly, the comparison between partial versus full interference patterns is difficult. However, the muscles on both sides of the larynx are normally activated to almost the same degree in different actions like respiration, phonation, and straining (3,5). Thus, in unilateral neurogenic lesions of the larynx, the detection of a significant difference in the interference pattern in identical muscles on both sides of the larynx can be considered as pointing to a neuropathic lesion of the muscle (Fig. 17). However, this observation is not constant. It also should be mentioned that the laryngeal paralysis varies considerably in degree and distribution among the different intrinsic laryngeal muscles. This may add to the discrepancy between the degree of denervation as detected from EMG and the e f f e c t i v e d i s p l a c e m e n t ( a d d u c t i o n abduction) of the vocal folds.

MUAP parameters and histograms The detection of spontaneous fibrillation potentials and the reduction of the number of the motor Journal of Voice, Vol. 6, No. 2, 1992

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M. N. KOTBY ET AL.

units on activation (reflected through interference patterns) are some of the most reliable features in diagnosis of neuromuscular pathologies (especially neurogenic lesions). These features cannot be used reliably in clinical laryngeal EMG. Accordingly, one is apt to rely heavily on the features (parameters) of the MUAPs. These MUAPs are known to show an increase in the mean duration and voltage in cases of neurogenic lesions. In laryngeal EMG, even this last mentioned pathological feature must be taken critically. MUAPs of laryngeal muscles are normally of short mean duration (2-4 ms) and small amplitude (150800 p~V) (Fig. 18). In neurogenic lesions, when the MUAPs show increase in mean duration and amplitude, they may still fall within the normal limits for a skeletal muscle. Accordingly, it is advisable, although time consuming, to measure these parameters and form a histogram for the pathological case to be represented on histograms of normal data (3,5) (Fig. 18).

INDICATIONS Early diagnosis of the nerve lesion Several authors consider laryngeal neuromyography the most useful tool in estimating the type and degree of laryngeal nerve injury shortly after its onset, far before it could be detected by EMG (8,11, 47). The evoked motor action potentials resulting from the stimulated nerve and the values of conduction velocity along the nerve give insight into the degree of damage, thus contributing to the prognosis and setting up of the policy of treatment. Diagnosis of the site of the nerve lesion In cases of neuropraxia or neurotemesis, before Wallerian degeneration sets in, the conduction velocity of the affected nerve will show a drop or a block proximal to the lesion, with normal conduction velocity distal to the lesion. Thus, neurographic studies may help to localize the site of lesion in the affected nerve (7,8,11,47,48).

NEUROGRAPHY (ENG) Monitoring the state of nerve regeneration

The concept of neuromyography is that stimulating a nerve and recording the electrically induced muscle activity of the innervated muscle will provide information about the neural integrity. In the case of EMG, the recorded muscle action potentials are either spontaneous or volitional, whereas for ENG, the muscle action potentials are only evoked potentials. Reflex myography, an entity of neuromyography, is the stimulation of an afferent sensory nerve with recording of the reflex muscular response.

After spontaneous recovery Satoh (47) stated that the evoked EMG test could reveal the state of spontaneous regeneration of the paralyzed laryngeal nerve as well as and even earlier than the ordinary EMG. After surgical reinnervation Many authors such as Crumley (25), Rice et al. (26), and Chang (50) used the evoked EMG test as an objective measure denoting the state of reinner-

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vation of the paralyzed laryngeal muscle using the different reinnervation techniques.

METHODOLOGY Peytz et al. (48) studied the nerve evoked action of the vocalis muscle in patients during total laryngectomy. They used a stainless steel needle (0.7 mm in diameter, 50 mm long), insulated except for 3 mm at the tip. For stimulation of the inferior laryngeal nerve they applied the active electrode peritracheal, and the reference electrode in the subcutaneous tissue of the jugular fossa, and for stimulation of the vagus nerve, they applied the active electrode just before the branching of the recurrent laryngeal nerve, with the reference electrode in the subcutaneous tissue anterior to the sternocleidomastoid muscle. They used stimuli of current pulses of 0.1 or 0.2 ms. The muscle response was picked up by concentric needle electrodes (0.45 mm in diameter), which were introduced either through a direct laryngoscope using local anesthesia and intravenous pethidine, or during total laryngectomy. Atkins (11), in his evoked EMG studies on dogs and humans, used a method similar to Peytz et al. (48) to obtain the human data. Satoh (47) used the evoked EMG test in their study on patients with recurrent laryngeal nerve paralysis. Stimulation was given to the internal branch of the superior laryngeal nerve, vagus nerve, and recurrent laryngeal nerve. The stimulating electrodes were made of copper wire (80 ~m in diameter, coated with enamel except for 5 mm along the edge). To stimulate the internal branch of the superior laryngeal nerve, both electrodes were inserted 1 cm deep and 1 cm apart in the thyrohyoid membrane with the point of nerve penetration between. To stimulate the recurrent nerve, the reference electrode was inserted 3 cm below the lower margin of the cricoid cartilage and the active electrode was inserted 1 cm above (both at a depth of 2.5 cm). To stimulate the vagus nerve, both electrodes were inserted 2.5 cm deep, at the external margin of the sternocleidomastoid muscle, with the reference electrode 1 cm above the active electrode at the same height of the electrodes used in stimulating the recurrent laryngeal nerve. These authors used a bipolar concentric needle electrode for recording, inserted via the percutaneous route into both the cricoarytenoid muscle and the thyroarytenoid muscle, representing the superior laryngeal and inferior la-

185

ryngeal nerve systems, respectively. They noticed that the threshold varied from 2 to 3 V when the stimulating electrode was relatively close to the nerve, up to 20 V when inserted seemingly distant from the nerve. Thumfart (8,51,52) used surface electrodes in stimulation of the superior laryngeal nerve in the region of its penetration through the thyrohyoid membrane. He used electric impulses of square waves of 0.5-1 ms and 50-80 V. The evoked muscle potentials were recorded by hooked wire or bipolar needle electrodes applied via direct route into the intrinsic laryngeal muscles, or via percutaneous route into the cricoarytenoid muscle. He also applied stimulations to the vagus and inferior laryngeal nerves during laryngectomies. Motor neurography was also performed by the same author, using a computer-aided method of electrostimulation (8). He used trains of 10, 20, and 50 pps for stimulation of the laryngeal nerves, with induction of a delay in the last stimulus in some cases. The neuromyographic responses obtained after the stimulation trains were digitalized and computed to get a widening of the response signal together with a recording of latency time, amplitude, and duration of the signal. Dejonckere (7) stimulated the superior laryngeal nerve (being easier to reach) using electric pulses of 1 ms and 5-50 V (which was found to vary according to the distance between the tip of the electrode and the nerve). The stimulation current intensity extended up to 1 mA and the frequency of impulses were one or two per second.

RESULTS Normal basic data Atkins (11), using EMG techniques to study laryngeal nerve conduction, confirmed that there is a 2- to 5-ms difference in latency between the left and fight recurrent laryngeal nerves with the conduction velocity the same bilaterally. The actual value varied, depending on the site of stimulation. He found the conduction velocity in the proximal portion of the recurrent laryngeal nerve to be 65 (-+5) m/s on the left and 63 (+5) m/s on the right, whereas the conduction velocity in the peripheral portion of the nerve was found to be 29 (-+3) m/s. These measurements confirmed previous data recovered by authors like Peytz et al. (48). Satoh (47), observed the following characteristics of the evoked waves in the laryngeal muscles after Journal of Voice, Vol. 6, No. 2, 1992

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M. N . K O T B Y E T A L .

stimulation of the corresponding laryngeal nerves. Stimulation of the internal branch of the superior laryngeal nerve induced a polyphasic potential in the cricothyroid muscle of 10-16 ms latency, 0.20.4 mV amplitude, and 6-7 ms duration. Stimulation of the vagus nerve induced a diphasic or triphasic potential in the thyroarytenoid muscle of 6-8 ms latency on the left side, 2-3 ms on the right side, amplitude of 0.4-0.7 mV and duration of 4-5 ms. As for the evoked waves induced from stimulating the recurrent laryngeal nerve, the latency recorded was 1.5-2.5 ms. It was diphasic or triphasic with 0.5-1.0 mV amplitude and 4-5 ms duration. Dejonckere (7) stated that at least 10 repetitive responses must be recorded in case of electroneurographic studies of the laryngeal nerve-muscle systems. He considered the second response after stimulation of the superior laryngeal nerve to be the true evoked potential, and the first to be an artifact caused by the passive stretching of the vocal folds due to the cricothyroid muscle contraction. Thumfart (8), by stimulating the superior laryngeal nerve in awake patients, recorded a first potential in the cricothyroid muscle after 4-6 ms and a second reflective potential in the same muscle after 16-18 ms. This second reflective potential (reflex myographic response) also could be measured from the posticus muscle and the vocalis muscle with a longer latency (22-24 ms after stimulation of the superior laryngeal nerve) depending on the side.

Pathological data On stimulation of the inferior laryngeal nerve or even the more difficult external laryngeal nerve, proximal to or at the site of the nerve lesion, there is a significant drop in the conduction velocity. The motor evoked response may also be dispersed, whereas stimulation distal to the nerve lesion will give normal figures. It should be pointed out, however, that the clinical application of the inferior laryngeal nerve and external laryngeal nerve stimulation is rather difficult. In cases of complete interruption of the laryngeal nerve or in degenerative palsies (of the axonotemesis type), after Wallerian degeneration has occurred, neither a neurogram nor a reflex myogram could be recorded from the larynx. While in cases of incomplete palsy of the recurrent laryngeal nerve (neurapraxia or axonotemesis before Wallerian degeneration), neuromyographic and reflex myographic responses of typical pathological patterns may be obtained. In these cases the latency of the Journal of Voice, Vol. 6, No. 2, 1992

FIG. 19. A new electrode for laryngeal EMG to solve the problem of electrode displacement (using a neutral hook) while keeping a fixed distance between the active poles as in concentric needle electrodes.

evoked potential increases, together with the duration (7,8,47). In reflex myography, lesions at any site of the reflex loop (superior laryngeal nerve, central connection, inferior laryngeal nerve) lead to an increase in the latency of the evoked motor response as well as widening (dispersion) of that response. REFERENCES 1. Feinstein B. The applications of electromyography to affections of the facial and the intrinsic laryngeal muscles. Proc R Soc Med 1946;39:817-8. 2. Faaborg-Andersen K. Electromyographic investigation of intrinsic laryngeal muscles in humans. Acta Physiol Scand [Suppl] 1957;41:140. 3. Kotby MN. Electromyography of the laryngeal muscles. [Thesis]. Cairo, Egypt: Ain Shams University, 1967. 4. Hirato J, Hirano M, Tomita H. Electromyographic investigation of human vocal cord paralysis. Ann Otol 1968;77:296304. 5. Kotby MN, Haugen LK. Clinical application of electromyography in vocal fold mobility disorders. Acta Otolaryngol Laryngol 1970;70:428-37. 6. Haglund S. Electromyography in the diagnosis of laryngeal motor disorders. Stockholm: Boktryckeri AB Thule, 1973. 7. Dejonckere PH. E.M.G. of the larynx. Louvain, Belgium: University of Louvain, 1987. 8. Thumfart WF. From larynx to vocal ability. New electrophysiological data. Acta Otolaryngol (Stockh) 1988;105:42531. 9. Dejonckere PH, Hamoir M. Etiologie des lesions neurogenes du larynx diagnostiqees electromyographiquement. Acta Otorhinolaryngol Belg 1980;34:285-99. 10. Hirano M, Shin T, Nozoe I. Prognostic aspects of recurrent laryngeal nerve paralysis. In: Buch NH, ed. Proceedings of the 17th Congress of Logopedics and Phoniatrics. Special Pedagogisk Forlag, Copenhagen, 1978;1:95-103. 11. Atkins JP. An electromyographic study of recurrent laryngeal nerve conduction and its clinical applications. Laryngoscope 1973;1:796-807. 12. Hirano M. Clinical examination of voice. New York: Springer Verlag, 1981. 13. Satoh J, Harvey J, Ogura H. Impairment of function of the intrinsic laryngeal muscles after regeneration of the recurrent laryngeal nerve. Laryngoscope 1974;84:53-66. 14. Hiroto I. Vocal cord paralysis. In: Fourteenth Congress of Logopedics and Phoniatrics. Interlaken, Karger, Basel 1976. 15. Colledge L, Ballance C. Treatment of paralysis of the diaphragms. Br Med J 1927;1:553-609.

ELECTROMYOGRAPHY AND NEUROGRAPHY 16. Siribodhi J, Sundmaher W, Atkins J, Bonner FJ. Electromyographic studies of laryngeal paralysis and regeneration of laryngeal motor nerves in dog. Laryngoscope 1963;73: 148-64. 17. Gordon HH, McCabe BF. The effect of accurate neurography on reinnervation and return of laryngeal function. Laryngoscope 1967;78:236-50. 18. Boles R, Fritzell B. Injury and repair of the recurrent laryngeal nerve in dogs. Laryngoscope 1969;79:1405-41. 19. Murakami Y, Kirchner JA. Vocal cord abduction with regenerated recurrent laryngeal nerve. Arch Otolaryngol 1971 ; 94:64-8. 20. Sato F, Ogura J. Neuroraphy of the recurrent laryngeal nerve. Laryngoscope 1978a;88:1034--41. 21. Tucker HH, Harvey JE, Ogura JH. Vocal cord remobilization in the canine larynx. Arch Otolaryngol 1970;92:530-3. 22. Tucker HH, Ogura JH. Vocal cord remobilization in the canine larynx. A historical evaluation. Laryngoscope 1971; 81:1602-6. 23. Sato F, Ogura H. Functional restoration for recurrent paralysis. An experimental study. Laryngoscope 1978b;88:85571. 24. Tucker HM. Human laryngeal reinnervation. Laryngoscope 1976;86:769-79. 25. Crumley RL. Experiments in laryngeal reinnervation. Laryngoscope 1982(suppl);92:1-27. 26. Rice DH, Owens O, Burstein F, Verity A. The nervemusclepedicle. Arch Otolaryngol 1983;109:233-4. 27. Ballance C. Results obtained in some experiments in which the facial and recurrent laryngeal nerves were anastomosed with other nerves. Br Med J 1924;2:349-54. 28. Iwamura S. Functioning remobilization of the paralyzed vocal cord in dogs. Arch Otolaryngol 1974;100:122-9. 29. Rice DH. Laryngeal reinnervation. Laryngoscope 1982;92: 1049-50. 30. Fex S. Function remobilization of vocal cords in cats with permanent recurrent laryngeal nerve paralysis. Acta Otolaryngol 1970;69:294-301. 31. Taggart JP. Laryngeal reinnervation by phrenic nerve implantation in dogs. Laryngoscope 1971;81:1330--6. 32. Moreledge D, Lauvestad WA, Calcaterra T. Delayed reinnervation of the paralysed larynx. Arch Otolaryngol 1973; 97:291-3. 33. Crumley RL. Phrenic nerve graft for bilateral vocal cord paralysis. Laryngoscope 1983;93:425-8. 34. Brondbo K, Hall C, Teig E, Dahl HA. Functional results after experimental reinnervation of the posterior cricoarytenoid muscle in dogs. J Otolaryngol 1986;15:259. 35. Dedo HH. Electromyography and visual evaluation of recur-

36. 37.

38. 39. 40. 41. 42. 43. 44. 45. 46. 47. 48. 49.

50. 51. 52.

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rent laryngeal nerve anastomosis in dogs. Ann Otolaryngology 1971 ;80:664-8. Dedo HH. The paralyzed larynx: an electromyographic study in dogs and humans. Laryngoscope 1970;80:1455-519. Blitzer A, Lovelace RE, Mitchell FB, Fahn S, Fink ME. Electromyographic findings in focal laryngeal dystonia (spastic dysphonia). Ann Otol Rhinol Laryngol 1985;94: 591--4. Kotby MN. Therapeutic considerations in the condition of sulcus glottidus. In: Proceedings of the 7th Congress of FALP. Special Pedagogisk for lag, Copenhagen, 1977. Thurmer S, Thumfart W, Kittel G. Elektromyographische Untersuchungsbefunde bei stottgeren. Sprache Stimme Grehor 1983;7:125-7. Hiroto I, Hirano M, Toyozumi Y, Shin I. Electromyographic investigation of the intrinsic laryngeal muscles related to speech sounds. Ann Otol Rhinol Laryngol 1967;76:861-72. Hirano M, Ohala J. Use of hooked-wire electrodes for electromyography of the intrinsic laryngeal muscles. J Speech Hear Res 1969;12:362-73. Knutsson E, Martensson A, Martensson B. The normal electromyogram in human vocal muscles. Acta Otolaryngol 1969;68:526-36. Kotby MM. Percutaneous laryngeal electromyography. Standardization of the technique. Folia Phoniatr 1975;27: 116-27. Merclis R. Electromyography. Acta Otorhinolaryngol Belg 1986;40:79-96. Goodgold J, Eberstein A. Electrodiagnosis of neuromuscular diseases. Baltimore, MD: Williams & Wilkins, 1972. Dedo HH, Hall W. Electrodes in laryngeal electromyography. Ann Otol Rhinol Laryngol 1969;78:172--81. Satoh I. Evoked electromyographic test applied for recurrent laryngeal paralysis. Laryngoscope 1978;88:2022-31. Peytz F, Rasmussen H, Buchtal F. Conduction time and velocity in human recurrent laryngeal nerve. Dan Med Bull 1965;12:125-7. Hughes GB, Josey AF, Glasscock ME, Jackson CG, Ray WA, Sismanis A. Clinical electroneurography: statistical analysis of controlled measurements in twenty-two normal subjects. Laryngoscope 1981 ;91:1834-46. Chang SY. Studies of early laryngeal reinnervation. Laryngoscope 1985;95:455-7. Thumfart WF. Endoscopic electromyography and neurography. In: Samii H, Janetta P J, eds. The cranial nerves. Berlin: Springer, 1981. Thumfart WF. Lupenendoskopische elektrodiagnostik Von Stimm-und Sprachstorunger. Sprache-Stimme Gehor 1983; 7:1-8.

Journal of Voice, Vol. 6, No. 2, 1992