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The neurology of stammering
Journal of Psychosomatic Research, Vol. 15, pp. 423
to 432.
Pergamon Press, 1971. Printed in Northern Ireland
THE NEUROLOGY
OF STAMMERING
BARRY WYKE*
MY PSYCHIATRICcolleagues have sometimes informed me that the performance of a succession of experiments by a scientist represents the acting-out of his particular As your guest, then, obsessive ritual in the womb-like environment of his laboratory. I must ask your indulgence if my obsessive personality impels me to take this opportunity of emerging from the womb to sprinkle a few drops of cold experimental rain on the lush, warm pastures of behaviouristic speculation in which we have been so happily browsing thus far at this meeting. In the circumstances of normal life there are but two ways in which the living brain may give overt display of its activity [I]. The first is a kind of chemical mode of expression, and consists of changes in glandular secretion-as when we weep for sorrow, or sweat with fear. The second, a mechanical mode of expression as it were, is manifest in changes of tension in visceral or voluntary muscles; and it is this latter mode that presumably concerns us at this Symposium on “Disorders of Movement”. These mechanical manifestations of the brain in action have a manifold significance : for in life the principal observable indices of nervous activity are presented by contraction and relaxation of striated muscles. Such phenomena thus provide the most tangible means of assessing the activity of the invisible, living brain. Furthermore, it is with his muscles that man ultimately establishes himself as a social organism, for they are the instruments by which he communicates his thoughts and feelings to his fellows and by which they, in their turn, convey their mind to him. In short, it is by their motility that we know the mind of others-a motility that involves principally the muscular apparatus of phonation, facial expression and limb movement. In man, then, it might be said that the cogitative functions of his brain ultimately fulfil themselves in the muscular activity of voluntary movement and postural adjustment. Thought and action become one, in so far as they are but two facets of the brain’s activity, the first being internal and private and the latter external and public. For whereas thought is a purely private and personal indication of his brain’s functioning to the introspective man, action-manifest as speech, gestures, movements or postural modifications-reveals to his fellows not only what he is thinking, but also, to a greater or lesser degree, the content and quality of his thought-and nowhere is this more true than in respect of the muscular activity involved in the act of speaking. From this it follows that any disorder of speech provides one of the most socially disabling afflictions to which a human being can be subject; and as one of the commonest disorders of speech in all communities is stammering [2], and as this particularly affects children during the period of acquirement of their mature speech patterns, it is obvious that a study of the mechanisms of stammering should be a matter of fundamental importance to those whose concern is with psychosomatic research. * Assisted by grants from the British Postgraduate Medical Federation of the University of London and the Camilla Samuel Fund. From The Neurological Laboratory, Royal College of Surgeons of England, London, England. 423
424
BARRY WYKE
In spite of its obvious magnitude as a clinical problem in most communities, however, stammering-like so much else in psychosomatics-has more often been the subject of empirical speculation than of scientific research, with the result that ideas as to its mode of production have often been esoteric in the extreme-ranging [3] from surgical suggestions that it results from structural abnormalities of the neuromuscular apparatus of the tongue to bizarre psycho-analytic proposals that it expresses a repressed wish to kill one’s auditor with words, or that it is a manifestation of persisting infantile oral exhibitionism or fetishism. But as so little is known of the precise physiological mechanisms involved in the normal act of phonation [4, 51, let alone in the disorder of this act that constitutes stammering [3], it is clear that no rational system of treatment of this latter disorder can be designed in the absence of such knowledge. As a first step in an attempt to remedy this unsatisfactory situation, I would like to lay before you at this meeting some neurological suggestions regarding the mechanisms that may underly the production of stammering, that have emerged as logical deductions from the experimental work on the neurology of phonation in which we are engaged in the Neurological Laboratory of the Royal College of Surgeons of England [3, 4, 6-101. At the outset, however, I must emphasize that these proposals-in so far as they relate to the clinical problem presented by the stammering patient-are tentative in the extreme, and are only intended to serve as a basis of discussion and to provide a substratum for further clinical research. They cannot be accepted until they are validated by direct comparative investigation of normal subjects and stammering patients-and although such an investigation is currently under way in my own laboratory it is only in its early stages, and we must await its outcome before we can determine the extent to which the proposals I am about to make are likely to apply in a clinical context. In considering the neurological substratum of stammering, we cannot do better than take as our starting point the definition of this affliction given in the Oxford English Dictionary-which, with its customary percipience, describes it as a disorder of articulation characterized by involuntary repetitions of a consonant or vowel before being able to pass to the following sound. Now the operative term in this definition is the word “involuntary’‘-which, to the neurologist, at once implies that the basis of the disorder is a disturbance of one or more of the reflex mechanisms that are involved in the production of normal speech; and indeed, this concept is the crux of the hypothesis that I wish to develop with you in this communication. It is not generally appreciated that the neuromuscular mechanisms involved in the production of speech are complex in the extreme, and comprise an array of reflex systems involved in the control of the respiratory, laryngeal, pharyngeal, glottal, mandibular and oral musculature, the continuously co-ordinated activity of which is the essential basis for the unconscious regulation of the rapid and precise changes in tone of the many muscles that are implicated in the act of speaking. The details of these many mechanisms need not concern us here, for I want to direct attention in this communication specifically to the reflex mechanisms that are involved in controlling the activity of the intrinsic muscles of the larynx-mechanisms that are clearly central to an understanding of the process of phonation and its disorders. Our investigations (Zoc. cit.) have established that there is a variety of mechanoreceptor nerve endings in the various tissues of the larynx-that is, in its mucous
The neurology of stammering
425
membrane, in the intrinsic muscles of the larynx themselves and in the capsules of the intercartilaginous joints of the larynx-the afferent discharges from which play a vital part in the reflex regulation of the activity of the intrinsic muscles of the larynx during respiration and phonation; and I now want to summarize for you some of the relevant observations in this regard, commencing with the laryngeal mucosal mechanoreceptors. Laryngeal nzucosal mechanoreceptors Although mechanoreceptors are found studded throughout the entire mucous lining of the larynx [3,4, 9-111, those implanted in the subglottic portion of the laryngeal mucous membrane are of special importance in the act of phonation-for here there is a dense array of slowly adapting mechanoreceptor nerve endings that have an extremely low threshold to mechanical deformation [3, 9, 12-151. Indeed, their threshold is so low that the frequency of their afferent discharges into the brain stem through the recurrent laryngeal nerve varies directly with the very small changes in subglottic air pressure that occur [16-191 in the normal act of respiration and, of course, during speech. This characteristic is illustrated in Fig. 1, which shows a recording from the afferent nerve fibres in the recurrent laryngeal nerve that innervate these subglottic mechanoreceptors. Here you can see that direction of a gentle puff of air onto the subglottic mucous membrane evokes a brief discharge of action potentials in the afferent nerve fibres innervating these receptors. As the subglottic air pressure rises and falls during the vocal expiratory air flow in normal speech, then, the frequency of the discharge from these mucosal mechanoreceptors is likewise increased or decreased; and when the former change occurs, the tone of the vocal fold adductors is reflexly increased (and that of the abductors is coincidentally decreased), so that the glottic orifice is narrowed and the tension in the vocal folds is increased with each elevation in subglottic air pressure, to a degree that is proportional to the magnitude of the change in air pressure. This reflex mechanism thus resists the separation and upward ballooning of the vocal folds that would otherwise be inevitable with each surge in vocal expiratory air pressure [3, 91.
FIG. 1. Afferent discharges in the distal cut end of the recurrent laryngeal nerve from low threshold subglottic mucosal mechanoreceptors. At the signal, a puff of air was directed from a fine catheter onto the subglottic surface of one vocal fold in the open larynx of an anaesthetized cat[l3].
BARRYWYKE
426
Laryngeal
myotatic
mechanoreceptors
Now let us consider the laryngeal myotatic mechanoreceptors-for it has often been stated that the intrinsic muscles of the larynx possess no such receptor mechanism [20,21]. However, investigations in the Anatomy Department of the Royal Free Hospital School of Medicine and in my own Laboratory (as well as elsewhere) have shown that this is not so, either in the cat or man [3,4, 7-10,22, 231. Indeed, the intrinsic muscles of the larynx are liberally provided with stretchsensitive mechanoreceptors of low threshold; but these receptor nerve endings for the most part consist of nerve fibres coiled round the individual muscle fibres of each intrinsic laryngeal muscle-such as you see in Fig. 2. In addition, there is a very small number of muscle spindles distributed in each of the intrinsic muscles of the larynx, one example of which can also be seen in Fig. 2. The fact that these nerve endings respond readily to mechanical stretch applied to the intrinsic muscles of the larynx is indicated in Fig. 3, which is a recording of the
L-l
50mV
1 sec.
FIG. 3.-Afferent discharges (in the internal laryngeal nerve) from stretch-sensitive mechanoreceptors in the ipsilateral vocalis muscle. The three recordings were made immediately before (A), immediately after (B) and 30 set after (C) the application of 10 g of stretch to the detached anterior end of the muscle in an anaesthetized cat[3]. nerve impulse traffic in the peripheral cut end of the recurrent laryngeal nerve evoked You can by the application of graduated stretch to an individual laryngeal muscle.
see that in these circumstances the mechanoreceptors within the muscle discharge impulses at increasing frequency into the afferent nerve fibres, which then relay them into the brain stem through the central connections of the laryngeal nerves. When this afferent volley reaches the motoneurones innervating the stretched muscle, their efferent discharge to the motor units in the muscle is augmented to produce an increase in tone in the muscle that opposes the applied stretch, as Fig. 4 shows.
to 432.
Pergamon Press, 1971. Printed in Northern Ireland
THE NEUROLOGY
OF STAMMERING
BARRY WYKE*
MY PSYCHIATRICcolleagues have sometimes informed me that the performance of a succession of experiments by a scientist represents the acting-out of his particular As your guest, then, obsessive ritual in the womb-like environment of his laboratory. I must ask your indulgence if my obsessive personality impels me to take this opportunity of emerging from the womb to sprinkle a few drops of cold experimental rain on the lush, warm pastures of behaviouristic speculation in which we have been so happily browsing thus far at this meeting. In the circumstances of normal life there are but two ways in which the living brain may give overt display of its activity [I]. The first is a kind of chemical mode of expression, and consists of changes in glandular secretion-as when we weep for sorrow, or sweat with fear. The second, a mechanical mode of expression as it were, is manifest in changes of tension in visceral or voluntary muscles; and it is this latter mode that presumably concerns us at this Symposium on “Disorders of Movement”. These mechanical manifestations of the brain in action have a manifold significance : for in life the principal observable indices of nervous activity are presented by contraction and relaxation of striated muscles. Such phenomena thus provide the most tangible means of assessing the activity of the invisible, living brain. Furthermore, it is with his muscles that man ultimately establishes himself as a social organism, for they are the instruments by which he communicates his thoughts and feelings to his fellows and by which they, in their turn, convey their mind to him. In short, it is by their motility that we know the mind of others-a motility that involves principally the muscular apparatus of phonation, facial expression and limb movement. In man, then, it might be said that the cogitative functions of his brain ultimately fulfil themselves in the muscular activity of voluntary movement and postural adjustment. Thought and action become one, in so far as they are but two facets of the brain’s activity, the first being internal and private and the latter external and public. For whereas thought is a purely private and personal indication of his brain’s functioning to the introspective man, action-manifest as speech, gestures, movements or postural modifications-reveals to his fellows not only what he is thinking, but also, to a greater or lesser degree, the content and quality of his thought-and nowhere is this more true than in respect of the muscular activity involved in the act of speaking. From this it follows that any disorder of speech provides one of the most socially disabling afflictions to which a human being can be subject; and as one of the commonest disorders of speech in all communities is stammering [2], and as this particularly affects children during the period of acquirement of their mature speech patterns, it is obvious that a study of the mechanisms of stammering should be a matter of fundamental importance to those whose concern is with psychosomatic research. * Assisted by grants from the British Postgraduate Medical Federation of the University of London and the Camilla Samuel Fund. From The Neurological Laboratory, Royal College of Surgeons of England, London, England. 423
424
BARRY WYKE
In spite of its obvious magnitude as a clinical problem in most communities, however, stammering-like so much else in psychosomatics-has more often been the subject of empirical speculation than of scientific research, with the result that ideas as to its mode of production have often been esoteric in the extreme-ranging [3] from surgical suggestions that it results from structural abnormalities of the neuromuscular apparatus of the tongue to bizarre psycho-analytic proposals that it expresses a repressed wish to kill one’s auditor with words, or that it is a manifestation of persisting infantile oral exhibitionism or fetishism. But as so little is known of the precise physiological mechanisms involved in the normal act of phonation [4, 51, let alone in the disorder of this act that constitutes stammering [3], it is clear that no rational system of treatment of this latter disorder can be designed in the absence of such knowledge. As a first step in an attempt to remedy this unsatisfactory situation, I would like to lay before you at this meeting some neurological suggestions regarding the mechanisms that may underly the production of stammering, that have emerged as logical deductions from the experimental work on the neurology of phonation in which we are engaged in the Neurological Laboratory of the Royal College of Surgeons of England [3, 4, 6-101. At the outset, however, I must emphasize that these proposals-in so far as they relate to the clinical problem presented by the stammering patient-are tentative in the extreme, and are only intended to serve as a basis of discussion and to provide a substratum for further clinical research. They cannot be accepted until they are validated by direct comparative investigation of normal subjects and stammering patients-and although such an investigation is currently under way in my own laboratory it is only in its early stages, and we must await its outcome before we can determine the extent to which the proposals I am about to make are likely to apply in a clinical context. In considering the neurological substratum of stammering, we cannot do better than take as our starting point the definition of this affliction given in the Oxford English Dictionary-which, with its customary percipience, describes it as a disorder of articulation characterized by involuntary repetitions of a consonant or vowel before being able to pass to the following sound. Now the operative term in this definition is the word “involuntary’‘-which, to the neurologist, at once implies that the basis of the disorder is a disturbance of one or more of the reflex mechanisms that are involved in the production of normal speech; and indeed, this concept is the crux of the hypothesis that I wish to develop with you in this communication. It is not generally appreciated that the neuromuscular mechanisms involved in the production of speech are complex in the extreme, and comprise an array of reflex systems involved in the control of the respiratory, laryngeal, pharyngeal, glottal, mandibular and oral musculature, the continuously co-ordinated activity of which is the essential basis for the unconscious regulation of the rapid and precise changes in tone of the many muscles that are implicated in the act of speaking. The details of these many mechanisms need not concern us here, for I want to direct attention in this communication specifically to the reflex mechanisms that are involved in controlling the activity of the intrinsic muscles of the larynx-mechanisms that are clearly central to an understanding of the process of phonation and its disorders. Our investigations (Zoc. cit.) have established that there is a variety of mechanoreceptor nerve endings in the various tissues of the larynx-that is, in its mucous
The neurology of stammering
425
membrane, in the intrinsic muscles of the larynx themselves and in the capsules of the intercartilaginous joints of the larynx-the afferent discharges from which play a vital part in the reflex regulation of the activity of the intrinsic muscles of the larynx during respiration and phonation; and I now want to summarize for you some of the relevant observations in this regard, commencing with the laryngeal mucosal mechanoreceptors. Laryngeal nzucosal mechanoreceptors Although mechanoreceptors are found studded throughout the entire mucous lining of the larynx [3,4, 9-111, those implanted in the subglottic portion of the laryngeal mucous membrane are of special importance in the act of phonation-for here there is a dense array of slowly adapting mechanoreceptor nerve endings that have an extremely low threshold to mechanical deformation [3, 9, 12-151. Indeed, their threshold is so low that the frequency of their afferent discharges into the brain stem through the recurrent laryngeal nerve varies directly with the very small changes in subglottic air pressure that occur [16-191 in the normal act of respiration and, of course, during speech. This characteristic is illustrated in Fig. 1, which shows a recording from the afferent nerve fibres in the recurrent laryngeal nerve that innervate these subglottic mechanoreceptors. Here you can see that direction of a gentle puff of air onto the subglottic mucous membrane evokes a brief discharge of action potentials in the afferent nerve fibres innervating these receptors. As the subglottic air pressure rises and falls during the vocal expiratory air flow in normal speech, then, the frequency of the discharge from these mucosal mechanoreceptors is likewise increased or decreased; and when the former change occurs, the tone of the vocal fold adductors is reflexly increased (and that of the abductors is coincidentally decreased), so that the glottic orifice is narrowed and the tension in the vocal folds is increased with each elevation in subglottic air pressure, to a degree that is proportional to the magnitude of the change in air pressure. This reflex mechanism thus resists the separation and upward ballooning of the vocal folds that would otherwise be inevitable with each surge in vocal expiratory air pressure [3, 91.
FIG. 1. Afferent discharges in the distal cut end of the recurrent laryngeal nerve from low threshold subglottic mucosal mechanoreceptors. At the signal, a puff of air was directed from a fine catheter onto the subglottic surface of one vocal fold in the open larynx of an anaesthetized cat[l3].
BARRYWYKE
426
Laryngeal
myotatic
mechanoreceptors
Now let us consider the laryngeal myotatic mechanoreceptors-for it has often been stated that the intrinsic muscles of the larynx possess no such receptor mechanism [20,21]. However, investigations in the Anatomy Department of the Royal Free Hospital School of Medicine and in my own Laboratory (as well as elsewhere) have shown that this is not so, either in the cat or man [3,4, 7-10,22, 231. Indeed, the intrinsic muscles of the larynx are liberally provided with stretchsensitive mechanoreceptors of low threshold; but these receptor nerve endings for the most part consist of nerve fibres coiled round the individual muscle fibres of each intrinsic laryngeal muscle-such as you see in Fig. 2. In addition, there is a very small number of muscle spindles distributed in each of the intrinsic muscles of the larynx, one example of which can also be seen in Fig. 2. The fact that these nerve endings respond readily to mechanical stretch applied to the intrinsic muscles of the larynx is indicated in Fig. 3, which is a recording of the
L-l
50mV
1 sec.
FIG. 3.-Afferent discharges (in the internal laryngeal nerve) from stretch-sensitive mechanoreceptors in the ipsilateral vocalis muscle. The three recordings were made immediately before (A), immediately after (B) and 30 set after (C) the application of 10 g of stretch to the detached anterior end of the muscle in an anaesthetized cat[3]. nerve impulse traffic in the peripheral cut end of the recurrent laryngeal nerve evoked You can by the application of graduated stretch to an individual laryngeal muscle.
see that in these circumstances the mechanoreceptors within the muscle discharge impulses at increasing frequency into the afferent nerve fibres, which then relay them into the brain stem through the central connections of the laryngeal nerves. When this afferent volley reaches the motoneurones innervating the stretched muscle, their efferent discharge to the motor units in the muscle is augmented to produce an increase in tone in the muscle that opposes the applied stretch, as Fig. 4 shows.