Examination of the relationships between jaw opener and closer rhythmical muscle activity in an in vitro brainstem jaw-attached preparation

An in vitro jaw-attached brainstem preparation was developed to investigate the relationship between jaw opener and closer muscle activity during chemically induced rhythmical jaw movements in neonatal rats. In the majority of preparations examined, where a defined region of brainstem was isolated and the neuronal innervation of the jaw opener and closer muscles was left intact, bath application of the excitatory amino acid agonist N -methyl-D,L-aspartate (NMA, 20-40 muM) in combination with bicuculline (BIC 10 muM), a GABAA antagonist, produced rhythmical electromyogram (EMG) activity in jaw opener and closer muscles, bilaterally, in conjunction with rhythmical jaw movements. Low concentrations of NMA (20 muM) in combination with BIC produced temporally coordinated activity between the jaw opener and closer muscles, ipsilaterally. With higher doses of NMA (40 muM), each muscle group exhibited bursting, but temporal coordination between them was difficult to establish. Similarly, NMA application in combination with the glycine antagonist strychnine (STR, 10 muM), also produced rhythmical EMG activity from both opener and closer muscles, ipsilaterally, but showed no temporal coordination between the antagonist muscle pair. However, coordination of opener and closer muscle discharge could be restored by the addition of BIC to the bath. We suggest that there exist separate, but coordinated, rhythm generator circuits for opener and closer motoneuronal discharge located in close proximity to the trigeminal motor nucleus and under GABAergic control for production of temporal coordination between rhythmogenic circuits.     

Changes in limb dynamics during the practice of rapid arm movements

In our study we examined Bernstein's hypothesis that practice alters the motor coordination among the muscular and passive joint moments. In particular, we conducted dynamical analyses of a human multisegmental movement during the practice of a task involving the upper extremity. Seven male human volunteers performed maximal-speed, unrestrained vertical arm movements whose upward and downward trajectories between two target endpoints required the hand to round a barrier, resulting in complex shoulder, elbow, and wrist joint movements. These movements were recorded by high-speed ciné film, and myopotentials from selected upper-extremity muscles were recorded. The arm was modeled as interconnected rigid bodies, so that dynamical interactions among the upper arm, forearm, and hand could be calculated. With practice, subjects achieved significantly shorter movement times. As movement times decreased, all joint-moment components (except gravity) increased, and the moment-time and EMG profiles were changed significantly. Particularly during reversals in movement direction, the changes in moment-time and EMG profiles were consistent with Bernstein's hypothesis relating practice effects and intralimb coordination: with practice, motor coordination was altered so that individuals employed reactive phenomena in such a way as to use muscular moments to counterbalance passive-interactive moments created by segment movements.     

High-Resolution,Non-Invasive Imaging of Upper Vocal Tract Articulators Compatible with Human Brain Recordings

A complete neurobiological understanding of speech motor control requires determination of the relationship between simultaneously recorded neural activity and the kinematics of the lips, jaw, tongue, and larynx. Many speech articulators are internal to the vocal tract, and therefore simultaneously tracking the kinematics of all articulators is nontrivial—especially in the context of human electrophysiology recordings. Here, we describe a noninvasive, multi-modal imaging system to monitor vocal tract kinematics, demonstrate this system in six speakers during production of nine American English vowels, and provide new analysis of such data. Classification and regression analysis revealed considerable variability in the articulator-to-acoustic relationship across speakers. Non-negative matrix factorization extracted basis sets capturing vocal tract shapes allowing for higher vowel classification accuracy than traditional methods. Statistical speech synthesis generated speech from vocal tract measurements, and we demonstrate perceptual identification. We demonstrate the capacity to predict lip kinematics from ventral sensorimotor cortical activity. These results demonstrate a multi-modal system to non-invasively monitor articulator kinematics during speech production, describe novel analytic methods for relating kinematic data to speech acoustics, and provide the first decoding of speech kinematics from electrocorticography. These advances will be critical for understanding the cortical basis of speech production and the creation of vocal prosthetics.     

Investigation of influencing variables on the computer-aided simulation of contacts in dynamic occlusion based on optically digitized plaster casts]

In dentistry, mechanical articulators with which mandibular movements can be reproduced in dentals casts play a major role. Commonly used semiadjustable articulators, however, have major limitations: On the one hand, the movement of the mandible is not reproduced exactly, on the other, they do not provide time-related information on jaw movement. Both problems can be solved by replacing the mechanical articulator by a digital simulation ("virtual articulator") based on digitized plaster casts and electronically recorded masticatory movements. We present a system for the 3D measurement of plaster casts in a skull-related, anatomical coordinate system using the fringe projection technique, and electronically recorded condylar movements. Using numerical algorithms, the contacts between upper and low jaw, and the angle of rotation of the temporomandibular joint can be computed for each movement in dynamic occlusion. Taking the data recorded from a patient as an example, the influence of the accuracy of the digitization of plaster casts on the computation of the rotation of the temporomandibular joint is discussed in relation to the anatomy of the masticatory apparatus.     

Stimulating the Lip Motor Cortex with Transcranial Magnetic Stimulation

Transcranial magnetic stimulation (TMS) has proven to be a useful tool in investigating the role of the articulatory motor cortex in speech perception. Researchers have used single-pulse and repetitive TMS to stimulate the lip representation in the motor cortex. The excitability of the lip motor representation can be investigated by applying single TMS pulses over this cortical area and recording TMS-induced motor evoked potentials (MEPs) via electrodes attached to the lip muscles (electromyography; EMG). Larger MEPs reflect increased cortical excitability. Studies have shown that excitability increases during listening to speech as well as during viewing speech-related movements. TMS can be used also to disrupt the lip motor representation. A 15-min train of low-frequency sub-threshold repetitive stimulation has been shown to suppress motor excitability for a further 15-20 min. This TMS-induced disruption of the motor lip representation impairs subsequent performance in demanding speech perception tasks and modulates auditory-cortex responses to speech sounds. These findings are consistent with the suggestion that the motor cortex contributes to speech perception. This article describes how to localize the lip representation in the motor cortex and how to define the appropriate stimulation intensity for carrying out both single-pulse and repetitive TMS experiments.     

Human Faces Are Slower than Chimpanzee Faces

Background

While humans (like other primates) communicate with facial expressions, the evolution of speech added a new function to the facial muscles (facial expression muscles). The evolution of speech required the development of a coordinated action between visual (movement of the lips) and auditory signals in a rhythmic fashion to produce “visemes” (visual movements of the lips that correspond to specific sounds). Visemes depend upon facial muscles to regulate shape of the lips, which themselves act as speech articulators. This movement necessitates a more controlled, sustained muscle contraction than that produced during spontaneous facial expressions which occur rapidly and last only a short period of time. Recently, it was found that human tongue musculature contains a higher proportion of slow-twitch myosin fibers than in rhesus macaques, which is related to the slower, more controlled movements of the human tongue in the production of speech. Are there similar unique, evolutionary physiologic biases found in human facial musculature related to the evolution of speech?

Methodology/Prinicipal Findings

Using myosin immunohistochemistry, we tested the hypothesis that human facial musculature has a higher percentage of slow-twitch myosin fibers relative to chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). We sampled the orbicularis oris and zygomaticus major muscles from three cadavers of each species and compared proportions of fiber-types. Results confirmed our hypothesis: humans had the highest proportion of slow-twitch myosin fibers while chimpanzees had the highest proportion of fast-twitch fibers.

Conclusions/significance

These findings demonstrate that the human face is slower than that of rhesus macaques and our closest living relative, the chimpanzee. They also support the assertion that human facial musculature and speech co-evolved. Further, these results suggest a unique set of evolutionary selective pressures on human facial musculature to slow down while the function of this muscle group diverged from that of other primates.     

Description of electromyograms using a mathematical model of single joint movement

A mathematical model for motor control over one-joint fast and slow movements is proposed based on the equilibrium point (EP) hypothesis. Equations describing a reaction of the muscle with its servo to an EP shift are presented. EMG level is estimated as a function of kinematic and control variables. Voluntary movements are performed by a ramp EP shift for the muscles subserving a given joint. EMG patterns obtained by a computer simulation are in good agreement with the experimental data.     

1998 ISEK Congress Keynote Lecture: Multi-muscle control in human movements

It has been suggested that the coordination of the activity of multiple muscles results from the comparison of the actual configuration of the body with a referent configuration specified by the nervous system so that the recruitment and gradation of the activity of each skeletal muscle depend on the difference between these two configurations. Active movements may be produced by the modification of the referent configuration. The hypothesis predicts the existence of a global minimum in electromyographic (EMG) activity of multiple muscles during movements involving reversals in direction. This prediction was tested in five subjects by analysing movements resembling the act of reaching for an object placed beyond one's reach from a sitting position. In such movements, initially sitting subjects raise their body to a semi-standing position and then return to sitting. Consistent with the hypothesis is the observation of a global minimum in the surface EMG activity of 16 muscles of the arm, trunk and leg at a specific phase of the movement. When the minimum occurred, EMG activity of each muscle did not exceed 2–7% of its maximal activity during the movement. As predicted, global EMG minima occurred at the phase corresponding to the reversal in movement direction, that is, during the transition from raising to lowering of the body. The global EMG minimum may represent the point at which temporal matching occurs between the actual and the referent body configurations. This study implies a specific link between motor behavior and the geometric shape of the body modified by the brain according to the desired action.     

Doublecortin is expressed in trigeminal motoneurons that innervate the velar musculature of lampreys: considerations on the evolution and development of the trigeminal system

Studies in lampreys have revealed interesting aspects of the evolution of the trigeminal system and the jaw. In the present study, we found a marker that distinguishes subpopulations of trigeminal motoneurons innervating two different kinds of oropharyngeal muscles. Immunofluorescence with an antibody against doublecortin (DCX; a neuron-specific phosphoprotein) enabled identification of the trigeminal motoneurons that innervate the velar musculature of larval and recently transformed sea lampreys. DCX-immunoreactive (-ir) motoneurons were observed in the rostro-lateral part of the trigeminal motor nucleus of these animals, but not in lampreys 1 month or more after metamorphosis. Combined double DCX/tubulin and serotonin/tubulin immunofluorescence and tract-tracing experiments with neurobiotin (NB) were also performed in larvae for further characterization of this system. Rich innervation by DCX-ir fibers was observed on the muscle fibers of the velum but not on the upper lip or lower lip muscles, which were innervated by tubulin-ir/DCX-negative fibers. No double-labelled DCX-ir motoneurons were observed in experiments in which the tracer NB was applied to the upper lip. Innervation of velar muscles by serotonergic fibers is also reported. The present results indicate that development of the trigeminal motoneurons innervating the velum differs from that of the trigeminal motoneurons innervating the lips, which is probably related to the dramatic regression of the velum during metamorphosis. The absence of data on a similar subsystem in the trigeminal motor nucleus of gnathostomes suggests that they may be lamprey-specific motoneurons. These results provide support for the "heterotopic theory" of jaw evolution and are inconsistent with the theories of a velar origin for the gnathostome jaw.     

Impedance characteristics of a neuromusculoskeletal model of the human arm I. Posture control

The mechanical impedance of neuromusculoskeletal models of the human arm is studied in this paper. The model analysis provides a better understanding of the contributions of possible intrinsic and reflexive components of arm impedance, makes clear the limitations of second-order mass-viscosity-stiffness models and reveals possible task effects on the impedance. The musculoskeletal model describes planar movements of the upper arm and forearm, which are moved by six lumped muscles with nonlinear dynamics. The motor control system is represented by a neural network which combines feedforward and feedback control. It is optimized for the control of movements or for posture control in the presence of external forces. The achieved impedance characteristics depend on the conditions during the learning process. In particular, the impedance is adapted in a suitable way to the frequency content and direction of external forces acting on the hand during an isometric task. The impedance characteristics of a model, which is optimized for movement control, are similar to experimental data in the literature. The achieved stiffness is, to a large extent, reflexively determined whereas the approximated viscosity is primarily due to intrinsic attributes. It is argued that usually applied Hill-type muscle models do not properly represent intrinsic muscle stiffness. Received: 14 October 1997 / Accepted in revised form: 18 May 1999     

Speech movements do not scale by orofacial structure size.

The potential role of a size-scaling principle in orofacial movements for speech was examined by using between-group (adults vs. 5-yr-old children) as well as within-group correlational analyses. Movements of the lower lip and jaw were recorded during speech production, and anthropometric measures of orofacial structures were made. Adult women produced speech movements of equal amplitude and velocity to those of adult men. The children produced speech movement amplitudes equal to those of adults, but they had significantly lower peak velocities of orofacial movement. Thus we found no evidence supporting a size-scaling principle for orofacial speech movements. Young children have a relatively large-amplitude, low-velocity movement strategy for speech production compared with young adults. This strategy may reflect the need for more time to plan speech movement sequences and an increased reliance on sensory feedback as young children develop speech motor control processes.     

Roles of dynamic and stationary components of a motor command in establishing the equilibrium state at simplest targeted movements

We studied in humans interrelations between the kinematic characteristics of targeted movements of the arm and current levels of EMG of the muscles providing these movements; the movements were relatively slow, and the attained joint angle was held for a time. The EMG level was considered a correlate of the level of integral motor commands (efferent activity of the respective motoneuronal pools). Application of low-amplitude non-inertial loadings, directed against the forces developed by one or another muscle group, allowed us to provide realization of targeted movements exclusively by the activity of this muscle group, without Involvement of the antagonists. It was demonstrated that the target equilibrium joint angle is reached synchronously with the dynamic phase of EMG activity, before the latter reaches a stationary level. The structure of the dynamic EMG phase itself is complex; in most cases it is split into several components. The dependence between the joint angle and amplitude of the EMG stationary phase is rather complex and variable, and usually it is difficult to predict the characteristics of this phase based on simple biomechanical considerations. There are proofs that at the performance of the studied movements and maintaining a target position there are some components in the mechanical muscle activity, which are not controlled by the motor commands. Thus, the stationary level of a motor command represents only one of several factors responsible for attaining and maintaining a target equilibrium position. Establishing this position is provided, first of all, by interaction of dynamic components of the motor commands to different muscles. Our results show that the attempts to interpret the processes of control of targeted movements on the basis of modifications of the equilibrium point hypothesis are inadequate; these data are in better compliance with the concept of impulse-temporal control; at their interpretation it is also necessary to take more thoroughly into account nonlinear properties of the muscle reactions.     

Further evaluation of an EMG technique for assessment of the deep cervical flexor muscles

A novel surface electromyographic (EMG) technique was recently described for the detection of deep cervical flexor muscle activity. Further investigation of this technique is warranted to ensure EMG activity from neighbouring muscles is not markedly influencing the signals recorded. This study compared deep cervical flexor (DCF) muscle activity with the activity of surrounding neck and jaw muscles during various anatomical movements of the neck and jaw in 10 volunteer subjects. DCF EMG activity was recorded with custom electrodes inserted via the nose and fixed by suction to the posterior mucosa of the oropharynx. Surface electrodes were placed over the sternocleidomastoid, anterior scalene, masseter and suprahyoid muscles. Positioned in supine, subjects performed isometric cranio-cervical flexion, cervical flexion, right and left cervical rotation, jaw clench and resisted jaw opening. Across all movements examined, EMG amplitude of the DCF muscles was greatest during neck movements that would require activity of the DCF muscles, particularly during cranio-cervical flexion, their primary anatomical action. The actions of jaw clench and resisted jaw opening demonstrated significantly less DCF EMG activity than the cranio-cervical flexion action (p < 0.05). Across all other movements, the neighbouring neck and jaw muscles demonstrated greatest EMG amplitude during their respective primary anatomical actions, which occurred in the absence of increased EMG amplitude recorded from the DCF muscles. The finding of substantial EMG activity of the DCF muscles only during neck actions that would require their activity, particularly cranio-cervical flexion, and not during actions involving the jaw, provide further assurance that the majority of myoelectric signals detected from the nasopharyngeal electrode are from the DCF muscles.     

Developmental fate of the mandibular mesoderm in the lamprey, Lethenteron japonicum: Comparative morphology and development of the gnathostome jaw with special reference to the nature of the trabecula cranii

The vertebrate jaw is a mandibular-arch derivative, and is regarded as the synapomorphy that defines the gnathostomes. Previous studies (Kuratani et al., Phil. Trans. Roy. Soc. 356:15, 2001; Shigetani et al., Science 296:1319, 2002) have suggested that the oral apparatus of the lamprey is derived from both the mandibular and premandibular regions, and that the jaw has arisen as a secondary narrowing of the oral patterning mechanism into the mandibular-arch domain. The heterotopy theory of jaw evolution states that the lamprey upper lip is a premandibular element, leaving further questions unanswered as to the homology of the trabecula in the lamprey and gnathostomes, and to the morphological nature of the muscles in the upper lip. Using focal injection of vital dyes into the cheek process core of lamprey embryos, we found that the upper lip muscle and trabecula are both derived from mandibular mesoderm. Secondary movement of the muscle primordium is also evident when the expression of the early muscle marker gene, LjMA2, is visualized. A nerve-fiber labeling study revealed that the upper lip muscle-innervating neurons are located in the rostral part of the brain stem, where the trigeminal motor nuclei are not found in gnathostomes. We conclude that the lamprey upper lip is composed of premandibular ectomesenchyme and a lamprey-specific muscle component derived from the mandibular mesoderm innervated by lamprey-specific motoneurons. Furthermore, the lamprey trabecula is most likely equivalent to a mesodermally derived neurocranial element, similar to the parachordal element in gnathostomes, rather than to the neural-crest-derived prechordal element.     

Electrophysiologic identification and evaluation of stylohyoid and posterior digastricus muscle complex.

PURPOSE: To identify the function of stylohyoid and posterior digastricus (STH-PD) muscle complex by the EMG techniques. METHODS: Unaffected sides of the faces of 30 patients with facial paralysis or hemifacial spasm were investigated. A concentric needle electrode was inserted to the STH-PD muscle complex and another concentric needle electrode was inserted to the orbicularis oris (OO) muscle. Simultaneous recording were obtained from two muscles using electrical stimulation (ES) (in 25 cases) and magnetic coil stimulation (MS) (in 15 cases); and both in 10 cases. Afterwards, the function of STH-PD was studied such as whistling, lip pursing, swallowing, jaw opening and closing. RESULTS: (1) The motor latency of compound muscle action potential (CMAP) of the STH-PD muscle was shorter than that of OO. (2) When the facial nerve was stimulated more distally than the stylomastoid foramen, the CMAP elicited from the STH-PD muscle complex immediately disappeared. (3) Ipsilateral MS was able to elicit the motor evoked potential (MEP) from STH-PD either at intracranially (half of cases) or at the extracranially. While OO muscle was always stimulated intracranially by MS. (4) The STH-PD muscle complex could not be basically recruited by the mimicry except lip pursing. The main recruitment were provided by swallowing and jaw opening. Cortical MS were facilitated during swallowing (5) Late reflex responses appeared in the STH-PD muscle complex during infraorbital-trigeminal and facial nerve ES. CONCLUSION: The STH-PD muscle complex is identified electrophysiologically. Although it is innervated by the facial nerve, its functions are mainly related with jaw opening and oropharyngeal swallowing. However, it is activated by the lip pursing.     

Cineradiography of monkey lip-smacking reveals putative precursors of speech dynamics

A key feature of speech is its stereotypical 5 Hz rhythm. One theory posits that this rhythm evolved through the modification of rhythmic facial movements in ancestral primates. If the hypothesis has any validity, then a comparative approach may shed some light. We tested this idea by using cineradiography (X-ray movies) to characterize and quantify the internal dynamics of the macaque monkey vocal tract during lip-smacking (a rhythmic facial expression) versus chewing. Previous human studies showed that speech movements are faster than chewing movements, and the functional coordination between vocal tract structures is different between the two behaviors. If rhythmic speech evolved through a rhythmic ancestral facial movement, then one hypothesis is that monkey lip-smacking versus chewing should also exhibit these differences. We found that the lips, tongue, and hyoid move with a speech-like 5 Hz rhythm during lip-smacking, but not during chewing. Most importantly, the functional coordination between these structures was distinct for each behavior. These data provide empirical support for the idea that the human speech rhythm evolved from the rhythmic facial expressions of ancestral primates.     

Jaw movement kinematics and jaw muscle (EMG) activity during drinking in the pigeon (Columba livia)

Summary Movements of the maxilla and mandible were recorded during drinking in the head-fixed pigeon and correlated with electromyographic activity in representative jaw muscle groups. During drinking, each jaw exhibits opening and closing movements along both the dorso-ventral and rostro-caudal axes which may be linked with or independent of each other. All subjects showed small but systematic increases in cycle duration over the course of individual drinking bouts. Cyclic jaw movements during drinking were correlated with nearly synchronous activity in the protractor (levator) of the upper jaw and in several jaw closer muscles, as well as with alternating activity in tongue protractor and retractor muscles. No EMG activity was ever recorded in the lower jaw opener muscle, suggesting that lower jaw opening in this preparation is produced, indirectly, by the contraction of other muscles. The results clarify the contribution of the individual jaws to the generation of gape variations during drinking in this species.Abbreviations AMEM adductor mandibulae externus muscle - DM depressor mandibulae muscle - EMG electromyographic - GENIO geniohyoideus muscle - LB lower beak - LED light-emitting diode - PQP protractor quadrati et pterygoidei muscle - PVL pterygoideus ventralis muscle, pars lateralis - SeH/StH serpihyoideus or stylohyoideus muscle - UB upper beak     

How does microgravity affect the muscular and kinematic synergies in a complex movement?

The planning and the execution of voluntary movement relies on sensorimotor transformations in which representations of the external environment are integrated into motor programs. We studied executions of Whole Body Pointing movements, in normal and in transient microgravity (parabolic flights) conditions. Three processes could lead to adaptation to the new environmental condition: a radical change of terrestrial synergies, their partial modification or preservation. By applying a multivariate analysis on kinematic and electromyographic (EMG) data and by comparing the 1g and 0g conditions, our findings hint the hypothesis the descending information from vestibular system may be directed to change the synergies' modulation. An analogous analysis was performed on the kinematics: the invariance of intersegmental coordination among the segments' elevation angles suggests that these kinematic waveforms are used as reference signals to determine the appropriate muscle synergies in a subordinate and flexible manner in order to adapt to the novel mechanical constraints.     

Control of jaw movements in two species of macropodines (Macropus eugenii and Macropus rufus).

The masticatory motor patterns of three tammar wallabies and two red kangaroos were determined by analyzing the pattern of electromyographic (EMG) activity of the jaw adductors and correlating it with lower jaw movements, as recorded by digital video and videoradiography. Transverse jaw movements were limited by the width of the upper incisal arcade. Molars engaged in food breakdown during two distinct occlusal phases characterized by abrupt changes in the direction of working-side hemimandible movement. Separate orthal (Phase I) and transverse (Phase II) trajectories were observed. The working-side lower jaw initially was drawn laterally by the balancing-side medial pterygoid and then orthally by overlapping activity in the balancing- and working-side temporalis and the balancing-side superficial masseter and medial pterygoid. Transverse movement occurred principally via the working-side medial pterygoid and superficial masseter. This pattern contrasted to that of placental herbivores, which are known to break down food when they move the working-side lower jaw transversely along a relatively longer linear path without changing direction during the power stroke. The placental trajectory results from overlapping activity in the working- and balancing-side adductor muscles, suggesting that macropods and placental herbivores have modified the primitive masticatory motor pattern in different ways.     

Control of jaw movements in two species of macropodines (Macropus eugenii and Macropus rufus)

The masticatory motor patterns of three tammar wallabies and two red kangaroos were determined by analyzing the pattern of electromyographic (EMG) activity of the jaw adductors and correlating it with lower jaw movements, as recorded by digital video and videoradiography. Transverse jaw movements were limited by the width of the upper incisal arcade. Molars engaged in food breakdown during two distinct occlusal phases characterized by abrupt changes in the direction of working-side hemimandible movement. Separate orthal (Phase I) and transverse (Phase II) trajectories were observed. The working-side lower jaw initially was drawn laterally by the balancing-side medial pterygoid and then orthally by overlapping activity in the balancing- and working-side temporalis and the balancing-side superficial masseter and medial pterygoid. Transverse movement occurred principally via the working-side medial pterygoid and superficial masseter. This pattern contrasted to that of placental herbivores, which are known to break down food when they move the working-side lower jaw transversely along a relatively longer linear path without changing direction during the power stroke. The placental trajectory results from overlapping activity in the working- and balancing-side adductor muscles, suggesting that macropods and placental herbivores have modified the primitive masticatory motor pattern in different ways.