The uniqueness of speech among motor systems

This paper considers evidence that the speech muscles are unique in their genetic, developmental, functional and phenotypical properties. The literature was reviewed using PubMed, ScienceDirect, ComDisDome and other literature-retrieval systems to identify studies reporting on the craniofacial and laryngeal muscles. Particular emphasis was given to studies of muscle fibre composition. A number of studies on mandibular, lingual, palatal and laryngeal muscles in humans show that these muscles are distinct from limb and other muscles. These speech-related muscles typically contain diverse fibre types and these types can vary regionally within a muscle. In general, the muscles of the speech production system are designed for fast and/or variable contraction and fatigue resistance. The craniofacial and laryngeal muscles are unique among the muscle systems of the human body and the specialized properties of these muscles are relevant to understanding the biomechanics of speech and various speech disorders.     

Spectral analyses of activity of laryngeal and orofacial muscles in stutterers.

Previous studies have reported that the disfluent speech of stutterers is often associated with tremor in orofacial muscle systems. In the present report, spectral analyses of the amplitude envelopes of laryngeal and orofacial EMGs revealed that tremor-like oscillations of EMG activity, similar to those observed in orofacial muscles, are also present in laryngeal muscles during stuttered speech. Furthermore, tremor-like oscillations in orofacial and laryngeal muscles appear to be entrained in some subjects. It is speculated that autonomic systems may provide a mechanism whereby oscillations in different muscle groups may become entrained.     

Intrinsic laryngeal muscles are spared from myonecrosis in the mdx mouse model of Duchenne muscular dystrophy

Intrinsic laryngeal muscles share many anatomical and physiological properties with extraocular muscles, which are unaffected in both Duchenne muscular dystrophy and mdx mice. We hypothesized that intrinsic laryngeal muscles are spared from myonecrosis in mdx mice and may serve as an additional tool to understand the mechanisms of muscle sparing in dystrophinopathy. Intrinsic laryngeal muscles and tibialis anterior (TA) muscle of adult and aged mdx and control C57Bl/10 mice were investigated. The percentage of central nucleated fibers, as a sign of muscle fibers that had undergone injury and regeneration, and myofiber labeling with Evans blue dye, as a marker of myofiber damage, were studied. Except for the cricothyroid muscle, none of the intrinsic laryngeal muscles from adult and old mdx mice showed signs of myofiber damage or Evans blue dye labeling, and all appeared to be normal. Central nucleation was readily visible in the TA of the same mdx mice. A significant increase in the percentage of central nucleated fibers was observed in adult cricothyroid muscle compared to the other intrinsic laryngeal muscles, which worsened with age. Thus, we have shown that the intrinsic laryngeal muscles are spared from the lack of dystrophin and may serve as a useful model to study the mechanisms of muscle sparing in dystrophinopathy.     

Involvement of fast and slow twitch muscle fibres in avian muscular dystrophy

The extent of differential fibre type involvement in chicken muscular dystrophy can be assessed quantitatively by the statistical parameters of fibre area, nuclei content and nuclei distribution in the individual fibre types. Two muscles, the posterior latissimus dorsi (PLD) and the serratus metapatagialis (SMP), were found to have similar overall fibre type composition, although the latter contains two subtypes of type I fibres, one of which has not previously been recognised in avian muscle. In both muscles, type IIB fibres are most affected by the progressive pathology. Nuclear proliferation is one of the histopathological features which can be measured, and in the PLD, the mean number of total nuclei in type IIB fibre cross-sections (N_t) is increased from 2.23 in normal chickens to 3.70 in dystrophic chickens, by 60 days. The corresponding values for N_t in type IIB muscle fibres of the SMP at 50 days are 1.74 and 5.10. Likewise, statistical analyses of the distribution of the fibre areas and their variability demonstrate that the incidence of abnormality in chicken dystrophy is greatest in type IIB fibres in both these muscles.Although type I fibres in the PLD are resistant to dystrophic change, it is noteworthy that in the SMP the type I fibres, also, are severely affected from an early stage, by these quantitative criteria. On the other hand, all fibres in a tonic muscle, the metapatagialis latissimus dorsi, are unaffected, as is true of all other tonic muscles previously studied. It is concluded that any twitch fibre type can, in principle, be affected by the actions of the gene concerned, and that this expression can be greatly modified in individual muscles by various physiological features, for example their natural pattern of use or relative disuse.     

Effects of age on enzyme-histochemical fibre spectra and contractile properties of fast- and slow-twitch skeletal muscles in the rat

Enzyme-histochemical fibre spectra and contractile properties were studied in fast-twitch (extensor digitorum longus (EDL) or tibialis anterior (TA)) and slow-twitch (soleus (S)) muscles of young adult (6 months) and old (20-24 months) male albino rats. It was found that ageing affected fibre size, fibre type proportions, and contractile properties of muscle tissue in both qualitative and quantitative terms and that these age-related alterations differed between fast- and slow-twitch muscles. In the fast-twitch TA and EDL, no differences were observed in either the total number of fibres, the cross-sectional area or the absolute and relative numbers of different muscle fibre types and subtypes between young adult and old animals. In the slow-twitch S, on the other hand, both the total number of muscle fibres and the average cross-sectional fibre area were smaller in the old animals. The fibre loss and fibre atrophy were most pronounced in type II fibres, especially type IIA. In TA, twitch force was higher and tetanus force was unaltered in the old as compared with the young adult animals, resulting in an increased twitch:tetanus ratio in old age. In S, on the other hand, both these forces were lower in the old animals and the twitch:tetanus ratio was accordingly unchanged with age. When the tetanus force was related to age-related differences in total muscle fibre cross-sectional area, no differences were found in the maximum force-generating capacity of maintained contractile material in either fast- or slow-twitch muscles between the two age groups. Probable mechanisms underlying the above alterations are discussed.     

The anatomy and fibre type composition of the human adductor pollicis in relation to its contractile properties

We have examined the anatomy and fibre type composition of the human adductor pollicis in muscles taken post mortem. Histochemical staining of muscle fibres showed that type I fibres predominated in all cases with a mean occurrence of 80%. This composition is similar to that of the soleus muscle and unlike that of the quadriceps which has approximately equal proportions of the two fibre types. Comparing the contractile characteristics, however, the adductor pollicis has similar properties to the quadriceps and both are quite distinct from those of the slowly contracting soleus muscle. The lack of correlation between fibre composition, as revealed by histochemical staining, and contractile properties in these muscles must mean that fibres of the same type from different muscles do not necessarily have the same contractile speed. The results also suggest that the type I fibres of the human adductor pollicis are faster than those of both the soleus and quadriceps muscles.     

Neurophysiologic markers in laryngeal muscles indicate functional anatomy of laryngeal primary motor cortex and premotor cortex in the caudal opercular part of inferior frontal gyrus

ObjectiveThe aim of this study was to identify neurophysiologic markers generated by primary motor and premotor cortex for laryngeal muscles, recorded from laryngeal muscle.MethodsTen right-handed healthy subjects underwent navigated transcranial magnetic stimulation (nTMS) and 18 patients underwent direct cortical stimulation (DCS) over the left hemisphere, while recording neurophysiologic markers, short latency response (SLR) and long latency response (LLR) from cricothyroid muscle. Both healthy subjects and patients were engaged in the visual object-naming task. In healthy subjects, the stimulation was time-locked at 10–300 ms after picture presentation while in the patients it was at zero time.ResultsThe latency of SLR in healthy subjects was 12.66 ± 1.09 ms and in patients 12.67 ± 1.23 ms. The latency of LLR in healthy subjects was 58.5 ± 5.9 ms, while in patients 54.25 ± 3.69 ms. SLR elicited by the stimulation of M1 for laryngeal muscles corresponded to induced dysarthria, while LLR elicited by stimulation of the premotor cortex in the caudal opercular part of inferior frontal gyrus, recorded from laryngeal muscle, corresponded to speech arrest in patients and speech arrest and/or language disturbances in healthy subjects.ConclusionIn both groups, SLR indicated location of M1 for laryngeal muscles, and LLR location of premotor cortex in the caudal opercular part of inferior frontal gyrus, recorded from laryngeal muscle, while stimulation of these areas in the dominant hemisphere induced transient speech disruptions.SignificanceDescribed methodology can be used in preoperative mapping, and it is expected to facilitate surgical planning and intraoperative mapping, preserving these areas from injuries.     

Morphology and ultrastructure of medial rectus subgroup motoneurons in the macaque monkey

There are two muscle fiber types in extraocular muscles: those receiving a single motor endplate, termed singly innervated fibers (SIFs), and those receiving multiple small terminals along their length, termed multiply innervated fibers (MIFs). In monkeys, these two fiber types receive input from different motoneuron pools: SIF motoneurons found within the extraocular motor nuclei, and MIF motoneurons found along their periphery. For the monkey medial rectus muscle, MIF motoneurons are found in the C‐group, while SIF motoneurons lie in the A‐ and B‐groups. We analyzed the somatodendritic morphology and ultrastructure of these three subgroups of macaque medial rectus motoneurons to better understand the structural determinants controlling the two muscle fiber types. The dendrites of A‐ and B‐group motoneurons lay within the oculomotor nucleus, but those of the C‐group motoneurons were located outside the nucleus, and extended into the preganglionic Edinger–Westphal nucleus. A‐ and B‐group motoneurons were very similar ultrastructurally. In contrast, C‐group motoneurons displayed significantly fewer synaptic contacts on their somata and proximal dendrites, and those contacts were smaller in size and lacked dense‐cored vesicles. However, the synaptic structure of C‐group distal dendrites was quite similar to that observed for A‐ and B‐group motoneurons. Our anatomical findings suggest that C‐group MIF motoneurons have different physiological properties than A‐ and B‐group SIF motoneurons, paralleling their different muscle fiber targets. Moreover, primate C‐group motoneurons have evolved a special relationship with the preganglionic Edinger–Westphal nucleus, suggesting these motoneurons play an important role in near triad convergence to support increased near work requirements. J. Comp. Neurol. 522:626–641, 2014. © 2013 Wiley Periodicals, Inc.     

Continuous myonuclear addition to single extraocular myofibers in uninjured adult rabbits

Extraocular muscles (EOM) are unique among mammalian skeletal muscles in that they normally express molecules associated with muscle development and regeneration. In this study we show that satellite cells of EOM, unlike those of other skeletal muscles, continually divide in the normal, uninjured adult. Adult EOM contained activated satellite cells positive for the myogenic regulatory factor MyoD. EOM satellite cells did not require a prolonged activation period prior to onset of cell division and differentiation in vitro. EOM satellite cells incorporated bromodeoxyuridine (brdU), a marker for cell division, and with longer postlabeling survival, brdU-labeled nuclei populated EOM myofibers. This was not seen with leg muscle. These findings suggest the possibility that continual division of satellite cells and fusion of their daughter myocytes with existing adult EOM myofibers contribute to the unique sparing or susceptibility of EOM to certain muscle diseases.     

Parabiotic reinnervation in normal and dystrophic mice. Part 2. Morphological studies.

The technique of parabiotic reinnervation has been used to test directly the neurogenic theory of the aetiology of muscular dystrophy in mice. Dystrophic muscles contain significantly fewer muscle fibres than their normal controls; they also have a much broader spectrum of fibre size because of a much higher proportion of very small fibres and are poorly differentiated into histochemical fibre types. These criteria were used to assess whether there was any amelioration of the dystrophic process in response to the introduction of a normal nerve supply, or whether dystrophic changes were induced in normal muscle reinnervated with a dystrophic nerve. Self-reinnervated normal and dystrophic TA and EDL muscles contained the same numbers of fibres as unoperated controls. The process of parabiosis alone resulted in no changes in normal or dystrophic muscles. In the process of parabiotic reinnervation, the efficiency of the reinnervation process was not affected by the parabiotic state. The parabiotic reinnervation of dystrophic muscle by normal nerve resulted in no significant increase in fibre numbers and the spectrum of fibre sizes was essentially the same as in unoperated dystrophic muscle. The parabiotic reinnervation of normal muscle by dystrophic nerve resulted in a reduction of fibre numbers in only some of the muscles examined. However, the spectrum of fibre diameters remained essentially normal, and the differentiation of the fibres into histochemical fibre types was characteristic of reinnervated normal muscle. There was a marked absence of necrosis or of other histological signs of dystrophy in these muscles. Since there was no positive evidence to show that conversion of normal to dystrophic, or dystrophic to normal muscle occurred under the influence of parabiotic nerve transposition, two alternative conclusions were admissible. Firstly, the influence of dystrophic nerve upon muscle may be operative in fetal or neonatal life and may be irreversible by means of the subsequent introduction of a normal nerve supply. Secondly, the dystrophic state in muscle may be determined by genetic factors independent of nerve supply.     

Laryngeal reflex regulation: Peripheral and central neural analyses

Because of the many functions (e.g., glottic closure, gagging, coughing, swallowing, speech) in which the internal laryngeal muscles are active, complex regulatory mechanisms must exist to modify and coordinate these activities. Little information is available, however, on these neural mechanisms, and the present study attempted to provide more information by investigating, in the adult cat, the effects of stimuli to various orofacial and upper respiratory tract sites and nerves on 110 single units recorded in individual laryngeal muscles, in the recurrent laryngeal nerve (RLN), and in the brain stem nucleus ambiguus. A particularly powerful excitatory influence on unitary activity related to laryngeal adduction was produced by laryngeal stimuli; in many instances this influence could not be modified by other sensory inputs (e.g., from vagus or glossopharyngeal nerves). Laryngeal stimulation also produced a profound cessation of respiration and suppression of the inspiratory-related activity of laryngeal abductor units. Excitatory and inhibitory effects as a result of interacting various stimuli were also seen in recordings from motoneurons of the RLN and nucleus ambiguus. The effects described show characteristics similar to those noted in other oral-facial muscles and indicate common integrative and regulatory mechanisms. This study in the adult cat provides a basis of comparison for future studies in the kitten where the effects of laryngeal stimulation are augmented to such an extent that they have been implicated in disorders such as the sudden infant death syndrome (SIDS).     

Effect of neurotrophin-3 on reinnervation of the larynx using the phrenic nerve transfer technique

Current techniques for reinnervation of the larynx following recurrent laryngeal nerve (RLN) injury are limited by synkinesis, which prevents functional recovery. Treatment with neurotrophins (NT) may enhance nerve regeneration and encourage more accurate reinnervation. This study presents the results of using the phrenic nerve transfer method, combined with NT-3 treatment, to selectively reinnervate the posterior cricoarytenoid (PCA) abductor muscle in a pig nerve injury model. RLN transection altered the phenotype and morphology of laryngeal muscles. In both the PCA and thyroarytenoid (TA) adductor muscle, fast type myosin heavy chain (MyHC) protein was decreased while slow type MyHC was increased. These changes were accompanied with a significant reduction in muscle fibre diameter. Following nerve repair there was a progressive normalization of MyHC phenotype and increased muscle fibre diameter in the PCA but not the TA muscle. This correlated with enhanced abductor function indicating the phrenic nerve accurately reinnervated the PCA muscle. Treatment with NT-3 significantly enhanced phrenic nerve regeneration but led to only a small increase in the number of reinnervated PCA muscle fibres and minimal effect on abductor muscle phenotype and morphology. Therefore, work exploring other growth factors, either alone or in combination with NT-3, is required.     

An immunocytochemical study of type I muscle fibres in developing human skeletal muscles

An immunocytochemical study was done on the skeletal muscles of human fetuses (19-36 weeks gestation), infants and adults using a new monoclonal antibody (McAb) ALD-47. The antibody was generated against slow myosin of chicken and is specific for myosin heavy chain (MHC). In human infants and adults the type I muscle fibres are strongly reactive with this McAb and the type II fibres uniformly non-reactive. In the fetuses from 19-20 weeks gestation (in whom the fibre types are not distinguishable by the histochemical myosin ATPase test) a proportion of muscle fibres react specifically with ALD-47. Other muscle fibres at this stage react positively with a fast specific MHC McAb HM-1.2 or are negative to both ALD-47 and HM-1.2 antibodies. These McAbs, thus, identify three distinct fibre populations in the early fetal muscle which by histochemical staining appears homogeneous. The percentage of ALD-47 positive fibres increases in fetuses at later gestational periods; at all stages these fibres lack reactivity with the HM-1.2 antibody. Because of its selective fibre type reactivity in differentiating muscles, the McAb ALD-47 in conjunction with HM-1.2 should be useful in immunoaffinity fractionation and biochemical studies of myosin isoforms in developing human muscles.     

EFFECTS OF DEXAMETHASONE ON FIBRE SUBTYPES IN RAT MUSCLE

Livingstone I., Johnson M.A. & Mastaglia F.L. (1981) Neuropathology and Applied Neurobiology 7, 381–398 Effects of dexamethasone on fibre subtypes in rat muscle The extent to which dexamethasone treatment produced atrophy of fast-twitch (EDL) and slow-twitch (SOL) muscles in the rat was investigated. The mean weight of steroid-treated EDL muscles was decreased as compared to normal, whereas SOL muscles from normal and dexamethasone-treated animals showed no significant difference. Muscle fibre diameters also showed comparatively minor changes in SOL, which consists of Type 1 (slow oxidative) and Type 2A (fast oxidative/glycolytic) fibres. Rat EDL contains, in addition to Type 1 and Type 2A fibres, two sub-populations of fast glycolytic fibres (Types 2B and 2B'). These fibre types showed the most severe degree of atrophy both after dexamethasone treatment and after denervation. The mean ratio of the weights of denervated to innervated EDL muscles was lower in steroid-treated rats than in normal animals suggesting that the atrophy produced by steroid treatment in conjunction with denervation was more than simply additive. Analysis of the proportions of histochemical fibre types in SOL and EDL showed that dexamethasone treatment produced no major alterations in the fibre type constitution of these muscles. However, further histochemical studies showed that there was relatively severe impairment of myophosphorylase activity in Type 2B' (fast glycolytic) fibres as compared to other fibre types; conversely Type 1 fibres frequently contained increased myophosphorylase. Levels of β-hydroxybutyrate dehydrogenase were low in both normal and steroid-treated EDL but high in SOL which also showed higher general oxidative activity. It is suggested that the particular susceptibility of fast glycolytic fibres to atrophy as a result of steroid treatment may be linked to: 1 the relatively severe reduction of myophosphorylase activity in these fibres and 2 their comparative inability to utilize alternative energy sources, especially substrates derived from free fatty acids.     

Denervation-induced region-specific changes in fibre types in the soleus and plantaris muscles of rats

Muscle fibre composition was compared among the proximal (25%), middle (50%) and distal (75%) regions of muscle to investigate whether denervation induces region-specific changes of fibre types in the soleus and plantaris muscles of rats. Decreases in mass were observed in both muscles after denervation. In the soleus muscle, denervation increased the percentage of type I fibres with a concomitant increase in the proportion of type IIC and IIA fibres. The extent of such transformations was greater in the proximal region than the middle and distal regions. In normal plantaris muscle, the middle region showed a higher proportion of type IIA fibres with a lower percentage of type IIB fibres reciprocally than other regions. These regional differences in fibre types were not detected in the 4-week denervated plantaris muscle. These findings suggest that denervation-induced transformations from type I to type II fibres begin in the proximal region in the soleus muscle of rats. In addition, regional differences in fibre types along the muscle length could be regulated by neuromuscular activity through normal innervation in the plantaris muscle. Received: 17 November 1995 / Revised: 29 April 1996 / Accepted: 15 July 1996     

Extraocular muscles: Morphogenetic study in humans light microscopy and ultrastructural features

Summary The development of human extraocular muscles (EOM) was studied in a series of fetal specimens (12–24 weeks gestation). EOM were evaluated by enzyme histochemistry (EZ) (NADH and ATPase), by differential phase contrast microscopy (DPC) and electron microscopy (EM). In the early fetus (14 weeks), there was no clear-cut sub-division into fibre types. A uniform histochemical reaction was seen with NADH while ATPase showed light and dark myotubes. Myotubes contained large central nuclei, prominent eccentric nucleoli, abundant glycogen granules, free ribosomes, numerous mitochondria, and dense and looser bundles of myofilaments. Mesenchymal cells undergoing mitosis and fibroblasts with prominent stacks of rough endoplasmic reticulum were scattered within endomysium. Mast cells with well formed cytoplasmic granules were found as early as 18–24 weeks. The same specimens by DPC showed differentiation into at least 4 different fibre types at 12 weeks. All the intramuscular nerves at 12–16 weeks were composed of unmyelinated fibres. At 18 weeks, myelinated axons were present. Morphologically immature end-plates devoid of junctional folds were found at 12 weeks. The motor innervation of some EOM appears to be derived from more than one axon (multiple innervated fibres). At 18 weeks gestational age, differentiation into fibre types became apparent by enzyme histochemistry. These histochemical and morphological findings suggest that morphologically mature endplates are not prerequisites for differentiation into muscle fibre types.     

Human vastus lateralis and gastrocnemius muscles. A comparative histochemical and biochemical analysis

Two muscles involved in locomotion the vastus lateralis and the gastrocnemius, were compared on a variety of histochemical an biochemical properties. Ten active males, age 20 - 24 years, served as subjects. Fibre type distributions, type I, type IIA and type IIB, as determined from samples extracted by muscle biopsy were similar in both muscles. In addition, no significant difference (p greater than 0.05) was found between fibre types in each muscle for fibre size, relative area, capillaries per fibre and the ratio of capillaries per fibre area. The activities of a number of enzymes representative of energy supplying pathways - the citric acid cycle (succinate dehydrogenase, SHD; beta-hydroxyacyl CoA dehydrogenase, HADH), glycogenolysis (total phosphorylase, PHOSP), glycolysis (phosphofructokinase, PFK) - were of similar magnitude between the two muscles. The only exception noted was for the activity of a glycolytic enzyme, lactate dehydrogenase, LDH, where a 16% higher value was observed in the vastus lateralis. The close degree of homogeneity displayed between these two muscles may be of significance in providing for a functional synchrony to occur in locomotor activities of varying intensity.     

The contribution of the interosseous muscles to the hypothenar compound muscle action potential

The contributions of the various ulnar‐innervated muscles of the hand to the hypothenar compound muscle action potential (CMAP) were estimated by directly stimulating individual muscles and by analyzing CMAP shape changes resulting from manipulations that changed individual muscle lengths. The results show that the first peak of the negative phase of the hypothenar CMAP comes from the hypothenar muscles, but that the second peak is due to a large volume‐conducted potential from the interosseous muscles. The interosseous contribution affects both the amplitude and the area of the CMAP, and makes these parameters sensitive to changes in the configuration of the fingers and the temperature gradient in the hand. To reduce the interosseous contribution, a “balanced reference” consisting of two reference electrodes, one over each tendon, is proposed. © 1999 John Wiley & Sons, Inc. Muscle Nerve 22: 6–15, 1999     

Organization of motor pools supplying the cervical musculature in a cryptodyran turtle, Pseudemys scripta elegans. II. Medial motor nucleus and muscles supplied by two motor nuclei

In this paper we describe the medial motor nucleus of Pseudemys cervical spinal cord and the motor pools of three neck muscles that exhibit an unusual pattern of innervation. Cells of the medial motor nucleus form a longitudinal column at the dorsomedial gray/white border of the ventral horn from C1 through C8. In Nissl-stained transverse sections they appear fusiform with prominent medially projecting dendrites; in HRP material these dendrites are seen to cross into the contralateral ventral funiculus. Medial nuclear cells vary in size (12-31 micron in diameter) and are often relatively large (greater than 21 micron in diameter). They are significantly larger and more numerous in caudal than in rostral cervical segments. Medial nuclear cells supply three of the cervical muscles examined in this study: mm. retrahens capitis collique (RCCQ), testocervicis, and longus colli. These three muscles differ from other cervical muscles in Pseudemys and from vertebrate limb muscles in that they are supplied in parallel by two populations of motor neurons: the medial and ventral motor nuclei (cf. Yeow and Peterson, '86). Ventral nuclear cells supplying these three muscles are organized into a musculotopic pattern with m. testocervicis motor neurons most medial and m. RCCQ motor neurons lateral; in contrast, the location of medial nuclear motor neurons is invariant with respect to muscle position. HRP-positive medial nuclear cells are sometimes smaller (m. testocervicis) but more often are as large or larger (mm. RCCQ and longus colli) than ventral nuclear cells supplying the same muscles, thus suggesting that they supply extrafusal muscle fibers, perhaps different muscle unit types in the three muscles. Based on the morphology of medial nuclear cells and the probable actions of the muscles they innervate, we hypothesize that the medial motor nucleus may represent a discrete functional system for producing bilaterally synchronous muscle activation, and that this system is accessed by a subset of muscles in the cervical complex.