Objective assessment of mandibular motor control using a 'reach-and-hold' task.

Mandibular motor function is well known to be impaired in the presence of temporomandibular disorders. However, while a vast literature is available concerning accuracy of motor control in limbs, quantitative and objective assessment of mandibular motor control has been seldom performed, also because of the lack of adequate investigative tools. Aim of this work is to present a technique for reliable evaluation of the motor performance of the mandible based on a kinesiography-monitored reach-and-hold task. Nineteen healthy subjects were engaged in a task in which they had to drive a cursor on a screen by corresponding movements of the mandible in the frontal plane and reach 30 random targets sequentially displayed on the screen. The whole task was repeated three times per session in two different days. The individual performance was assessed by different indices evaluating precision and steadiness of target matching. The performance progressively improved in the three trials of the first session, further improved and stabilised in the second session, with an average positioning error of 0·59 ± 038 mm and was slightly correlated with the horizontal dimension of the mandible border movement (r = 0·55). Intraclass correlation coefficient ranged between 0·76 and 0·94 for the different indices indicating good repeatability. The kinesiographic technique allowed for objective and reliable assessment of the voluntary control of the mandible position. Its potential applications include support to the characterisation of temporomandibular disorders and to motor training and progress monitoring in rehabilitation treatments.

On whether there is a direct sympathetic influence on jaw muscle spindles.

Electric stimulation of the peripheral stump of cervical sympathetic nerve (0.5-5.0 sec trains at 1 msec, 6-10 V, 0.5-30 HZ) induced in jaw muscle spindle afferents: (1) decrease of discharge frequency with 0.6-2.5 sec latency, lasting 8-13 sec (in 40% of the units) possibly due to direct sympathetic innervation of spindles; and (2) subsequent modest increase of frequency, probably secondary to muscular vasoconstriction.

Sympathetic control of skeletal muscle function: possible co-operation between noradrenaline and neuropeptide Y in rabbit jaw muscles.

Stimulation of the cervical sympathetic nerve at 10/s increases by 12.9 +/- 0.7% peak tension of maximal twitches in the directly stimulated jaw muscles and markedly depresses (41.6 +/- 1.3%) the tonic vibration reflex (TVR) elicited in the same muscles by vibration of the mandible. Both effects are not significantly influenced by administration of beta-adrenoceptor antagonists. When both alpha- and beta-adrenergic receptors are blocked, sympathetic stimulation induces a very small increase in twitch tension (3.8 +/- 0.7%), while no detectable change in the TVR is observed. Close arterial injection of alpha 1-adrenoceptor agonist phenylephrine mimics the effects induced by sympathetic stimulation on twitch tension and TVR, dose-dependently. The noradrenaline co-transmitter neuropeptide Y also produces a long-lasting, dose-dependent increase in the twitch tension which is unaffected by blockade of adrenergic receptors as well as of the neuromuscular junctions. Contribution of neuropeptide Y to the sympathetically-induced reduction of the stretch reflex is not clearly demonstrated. These data suggest that co-operation between noradrenaline and neuropeptide Y may be effective in determining sympathetic modulation of skeletal muscle function.

Spontaneous sympathetic command to skeletal muscles: functional implications.

The sympathetic system can influence skeletal muscle function through an action exerted at the peripheral level, namely on muscle spindle afferent information and muscular contraction. Data supporting such a conclusion are briefly reviewed. Also, the results described in the present paper suggest that the sympathetic nervous command affecting muscle function is tonic in nature and that it can be modulated by inputs which are known to influence other sections of the sympathetic system.

Effect of cervical sympathetic nerve stimulation on nociceptive jaw opening reflex in the cat.

In anaesthetized cats the electrical stimulation of the cervical sympathetic nerve induces a considerable increase (150-250%) in the nociceptive jaw opening reflex elicited by tooth pulp stimulation (JOR). The mechanisms potentially responsible for this effect are discussed and the possibility is suggested, that a portion of the response is due to a modulatory action exerted by the sympathetic on the nociceptive input.

Sympathetic modulation of periodontal mechanoreceptors.

The effect of the electrical stimulation of the peripheral stump of the cervical sympathetic nerve, at physiological frequencies, was studied on the activity of mechanoreceptors with sensory field around the teeth, in anaesthetized and paralysed animals. In the 33% of the tested units either an increase of the resting discharge rate or an activation of the receptors occurred. The latency of this response ranged between 0.3 and 6 sec; the maximum discharge frequency, which varied widely in different units, was reached within the subsequent 2 to 4 sec and usually outlasted the duration of the stimulation. The possible mechanisms of this sympathetic effect are discussed on the basis of its latency and pattern and of the following further observations: i) its presence after denervation of carotid sinus and glomus, ii) its dependence on the stimulation of preganglionic sympathetic fibres belonging to the groups S1 and S2, iii) the absence of response in the mechanoreceptor units by the temporary occlusion of the ipsilateral common carotid artery.

Modulation of the jaw jerk reflex by the sympathetic nervous system.

The effect of sympathetic stimulation on the jaw jerk reflex has been studied in precollicular decerebrate rabbits. This reflex was elicited by a downward mandibular movement applied to the lower jaw through a servo controlled puller. Unilateral stimulation of the cervical sympathetic nerve at 10/s consistently induced a decrease in the JJR, i.e. a marked reduction of the EMG activity in the ipsilateral masseter muscle, accompanied by a 30-40% decrease in the reflexly developed force. In these trials EMG of the contralateral muscle, recorded as control, was not significantly affected. Bilateral stimulation of cervical sympathetic nerve strongly reduced or suppressed the EMG activity in both sides and produced a parallel decrease in the developed force which reached values ranging from 12.5% to 37.0% of controls (with an average of 28.9% +/- 8.9, S.D.). The effect of sympathetic stimulation was also tested on the contraction of the masseter muscle elicited by direct electrical stimulation. Sympathetic activation induced a modest increase in both amplitude and duration of muscle twitch, thus showing that the reduction in the reflex response can not be attributed to an action exerted by the adrenergic mediator on the muscular contraction. All these effects were almost completely abolished by the blockade of alpha-adrenergic receptors. They were proved not to be secondary to the sympathetically-induced vasomotor changes. Therefore the marked JJR reduction produced by activation of the sympathetic nervous system is suggested to be due to the sympathetically-induced decrease in neuromuscular spindle sensitivity to muscle length changes, previously reported.

Localization of neurons innervating masticatory muscle spindle and periodontal receptors in the mesencephalic trigeminal nucleus and their reflex actions.

The mesencephalic trigeminal nucleus was studied in anaesthetized and curarized rabbits by recording the unitary activity through extracellular microelectrodes and identifying the constituent cell types. Two types of units were found, namely primary afferents supplying jaw raising muscle spindles and periodontal or gingival mechanoreceptors. These two groups of neurons exhibited a rostrocaudal somatotopy: the former occupied the entire rostral portion of the nucleus (A7-P2.3; trochlear decussation being taken as an arbitrary 0 level), the latter was located caudally (P3-P4.5) while the somata of both types of afferent fibres were present between P2.2 and P3. No evidence was found for representation of both tendon organs of jaw muscles and joint receptors. Among the units innervating muscle spindles, secondary afferents were largely more numerous than the primary ones. Among periodontal and gingival mechanoreceptor afferents, incisors were the most widely represented, followed by interalveolar gingiva and molars; the axonal conduction velocity ranged between 9 and 40 m/sec and between 8 and 16 m/sec for ipsilaterally and contralaterally projecting neurons, respectively. The motor responses obtained by electrical stimulation of discrete areas of the MTN confirmed the presence of a high degree of segregation between the two different populations of neurons. In fact, jaw raising movements are obtained when stimulating the area within A7 and P2 containing the somata of spindle afferent neurons, while only jaw opening movements are elicited by stimulation of the caudal levels of the nucleus. These data also show that the periodontal neurons whose somata are located in the MTN participate in the jaw opening reflex, just as the more numerous periodontal mechanoreceptors whose somata are located in the Gasser ganglion. Soma-somatic and soma-axon hillock gap junctions were found among the neurons of the MTN, particularly in the caudal third of the nucleus.

Responses of muscle spindles in feline dorsal neck muscles to electrical stimulation of the cervical sympathetic nerve.

Previous studies performed in jaw muscles of rabbits and rats have demonstrated that sympathetic outflow may affect the activity of muscle spindle afferents (MSAs). The resulting impairment of MSA information has been suggested to be involved in the genesis and spread of chronic muscle pain. The present study was designed to investigate sympathetic influences on muscle spindles in feline trapezius and splenius muscles (TrSp), as these muscles are commonly affected by chronic pain in humans. Experiments were carried out in cats anesthetized with alpha-chloralose. The effect of electrical stimulation (10 Hz for 90 s or 3 Hz for 5 min) of the peripheral stump of the cervical sympathetic nerve (CSN) was investigated on the discharge of TrSp MSAs (units classified as Ia-like and II-like) and on their responses to sinusoidal stretching of these muscles. In some of the experiments, the local microcirculation of the muscles was monitored by laser Doppler flowmetry. In total, 46 MSAs were recorded. Stimulation of the CSN at 10 Hz powerfully depressed the mean discharge rate of the majority of the tested MSAs (73%) and also affected the sensitivity of MSAs to sinusoidal changes of muscle length, which were evaluated in terms of amplitude and phase of the sinusoidal fitting of unitary activity. The amplitude was significantly reduced in Ia-like units and variably affected in II-like units, while in general the phase was affected little and not changed significantly in either group. The discharge of a smaller percentage of tested units was also modulated by 3-Hz CSN stimulation. Blockade of the neuromuscular junctions by pancuronium did not induce any changes in MSA responses to CSN stimulation, showing that these responses were not secondary to changes in extrafusal or fusimotor activity. Further data showed that the sympathetically induced modulation of MSA discharge was not secondary to the concomitant reduction of muscle blood flow induced by the stimulation. Hence, changes in sympathetic outflow can modulate the afferent signals from muscle spindles through an action exerted directly on the spindles, independent of changes in blood flow. It is suggested that such an action may be one of the mechanisms mediating the onset of chronic muscle pain in these muscles in humans.

Effects of sympathetic stimulation on the rhythmical jaw movements produced by electrical stimulation of the cortical masticatory areas of rabbits.

The somatomotor and sympathetic nervous systems are intimately linked. One example is the influence of peripheral sympathetic fibers on the discharge characteristics of muscle spindles. Since muscle spindles play important roles in various motor behaviors, including rhythmic movements, the working hypothesis of this research was that changes in sympathetic outflow to muscle spindles can change rhythmic movement patterns. We tested this hypothesis in the masticatory system of rabbits. Rhythmic jaw movements and EMG activity induced by long-lasting electrical cortical stimulation were powerfully modulated by electrical stimulation of the peripheral stump of the cervical sympathetic nerve (CSN). This modulation manifested itself as a consistent and marked reduction in the excursion of the mandibular movements (often preceded by a transient modest enhancement), which could be attributed mainly to corresponding changes in masseter muscle activity. These changes outlasted the duration of CSN stimulation. In some of the cortically evoked rhythmic jaw movements (CRJMs) changes in masticatory frequency were also observed. When the jaw-closing muscles were subjected to repetitive ramp-and-hold force pulses, the CRMJs changed characteristics. Masseter EMG activity was strongly enhanced and digastric EMG slightly decreased. This change was considerably depressed during CSN stimulation. These effects of CSN stimulation are similar in sign and time course to the depression exerted by sympathetic activity on the jaw-closing muscle spindle discharge. It is suggested that the change in proprioceptive information induced by an increase in sympathetic outflow (a) has important implications even under normal conditions for the control of motor function in states of high sympathetic activity, and (b) is one of the mechanisms responsible for motor impairment under certain pathological conditions such as chronic musculoskeletal head-neck disorders, associated with stress conditions.

A dual effect of sympathetic nerve stimulation on jaw muscle spindles.

In anaesthetized and paralyzed rabbits, electrical stimulation of the cervical sympathetic nerve at physiological frequencies induces in jaw muscle spindle afferents a short-latency decrease or suppression of discharge. This effect is very stereotyped in pattern and is attributed to direct sympathetic innervation of spindles. It is mediated by preganglionic S1-S2 sympathetic fiber groups. A longer-latency facilitatory effect follows, probably vasomotor in origin and mediated by S3-S4 groups. Both responses are eliminated by administration of alpha-adrenergic blocking agents. The latencies, patterns, thresholds, durations and reproducibility of these responses have been studied and the mechanisms possibly involved are discussed.

Effect of sympathetic nervous system activation on the tonic vibration reflex in rabbit jaw closing muscles.

1. In precollicular decerebrate rabbits we investigated the effect of sympathetic stimulation, at frequencies within the physiological range, on the tonic vibration reflex (TVR) elicited in jaw closing muscles by small amplitude vibrations applied to the mandible (15-50 microns, 150-180 Hz). The EMG activity was recorded bilaterally from masseter muscle and the force developed by the reflex was measured through an isometric transducer connected with the mandibular symphysis. 2. Unilateral stimulation of the peripheral stump of the cervical sympathetic by the TVR, and a marked decrease or disappearance of the ipsilateral EMG activity. No significant changes were detected in the EMG contralateral to the stimulated nerve. Bilateral CSN stimulation reduced by 60-90% the force reflexly produced by the jaw closing muscles and strongly decreased or suppressed EMG activity on both sides. This effect was often preceded by a transient TVR enhancement, very variable in amplitude and duration, which was concomitant with the modest increase in pulmonary ventilation induced by the sympathetic stimulation. 3. During bilateral CSN stimulation, an increase in the vibration amplitude by a factor of 1.5-2.5 was sufficient to restore the TVR reduced by sympathetic stimulation. 4. The depressant action exerted by sympathetic activation on the TVR is mediated by alpha-adrenergic receptors, since it was almost completely abolished by the I.V. administration of either phentolamine or prazosin, this last drug being a selective antagonist of alpha 1-adrenoceptors. The sympathetically induced decrease in the TVR was not mimicked by manoeuvres producing a large and sudden reduction or abolition of the blood flow to jaw muscles, such as unilateral or bilateral occlusion of the common carotid artery. 5. The effect of sympathetic stimulation was not significantly modified after denervation of the inferior dental arch and/or anaesthesia of the temporomandibular joint, i.e. after having reduced the afferent input from those receptors, potentially affected by CSN stimulation, which can elicit either a jaw opening reflex or a decrease in the activity of the jaw elevator muscle motoneurons. 6. These data suggest that, when the sympathetic nervous system is activated under physiological conditions, there is a marked depression of the stretch reflex which is independent of vasomotor changes and is probably due to a decrease in sensitivity of muscle spindle afferents.

Postsynaptic alpha 1- and alpha 2-adrenoceptors mediating the action of the sympathetic system on muscle spindles, in the rabbit.

In anaesthetized and curarized rabbits, the cervical sympathetic nerve (CSN) stimulation induces in jaw elevator muscles a tension response which can be mimicked by the intravenous injection of adrenaline, noradrenaline and phenylephrine. This response, previously described and attributed to the contraction of muscle spindle fibres, is entirely mediated by alpha-adrenoceptors. The administration of phenoxybenzamine (2.5-3.5 mg/kg) markedly inhibits the responses to the sympathetic stimulation and to the injection of adrenergic agonists. Rauwolscine (1 mg/kg) reduces the development of tension induced by both CSN stimulation and noradrenaline injection without significantly affecting the response to phenylephrine. These data suggest the presence of postsynaptic alpha 1- and alpha 2-adrenoceptors in intrafusal muscle fibres. Moreover, the possibility that alpha 2-adrenoceptors may also have an extrasynaptic location is entertained.

A comparative study of changes operated by sympathetic nervous system activation on spindle afferent discharge and on tonic vibration reflex in rabbit jaw muscles.

The effect of sympathetic activation on the spindle afferent response to vibratory stimuli eliciting the tonic vibration reflex in jaw closing muscles was studied in precollicularly decerebrate rabbits. Stimulation of the cervical sympathetic trunk, at frequencies within the physiologic range, consistently induced a decrease in spindle response to muscle vibration, which was often preceded by a transient enhancement. Spindle discharge was usually correlated with the EMG activity in the masseter muscle and the tension reflexly developed by jaw muscles. The changes in spindle response to vibration were superimposed on variations of the basal discharge which exhibited different patterns in the studied units, increases in the firing rate being more frequently observed. These effects were mimicked by close arterial injection of the selective alpha 1-adrenoceptor agonist phenylephrine. Data presented here suggest that sympathetically-induced modifications of the tonic vibration reflex are due to changes exerted on muscle spindle afferent information.

Sympathetically-induced development of tension in jaw muscles: the possible contraction of intrafusal muscle fibres.

In rabbits, cats and rats anaesthetized, curarized, with the skull fixed in a stereotaxic apparatus, the peripheral stump of the cervical sympathetic nerve (c.s.n.) was electrically stimulated at frequencies within the physiological range and the isometric tension was recorded at the lower jaw. In a group of experiments the afferent discharge from the jaw elevator muscle spindles was also recorded, in the mesencephalic nucleus of the fifth cranial nerve. Unilateral stimulation of the c.s.n. induced in jaw elevator muscles of rabbits an increase of tension of 5.5 +/- 0.5 g (latency: 0.5-2 s, time constant: 2.5-5 s) maintained with little or no decrement until the end of stimulation. This response proved not to be secondary to vasomotor changes since: i) approximately half of it was mediated by the fastest conducting component of the c.s.n. fibres, ii) it was not mimicked by a sudden reduction of blood supply to the muscles, iii) it was unaffected by 10 min bilateral occlusion of both the external and the internal carotid arteries. During c.s.n. stimulation the afferent discharge from spindles belonging to jaw elevator muscles exhibited an increase of firing (often preceded by a transient decrease) lasting throughout the stimulation. Also, the position sensitivity of all the spindle afferents tested was modified by the sympathetic stimulation. The results presented are interpreted to suggest that the sympathetic system may induce an intrafusal muscle fibre contraction in jaw elevator muscles. The possible functional implications are also discussed.

Sympathetic modulation of muscle spindle afferent sensitivity to stretch in rabbit jaw closing muscles.

Previous reports showed that sympathetic stimulation affects the activity of muscle spindle afferents (MSAs). The aim of the present work is to study the characteristics of sympathetic modulation of MSA response to stretch: (i) on the dynamic and static components of the stretch response, and (ii) on group Ia and II MSAs to evaluate potentially different effects. In anaesthetised rabbits, the peripheral stump of the cervical sympathetic nerve (CSN) was stimulated at 10 impulses s(-1) for 45-90 s. The responses of single MSAs to trapezoidal displacement of the mandible were recorded from the mesencephalic trigeminal nucleus. The following characteristic parameters were determined from averaged trapezoidal responses: initial frequency (IF), peak frequency at the end of the ramp (PF), and static index (SI). From these, other parameters were derived: dynamic index (DI = PF - SI), dynamic difference (DD = PF - IF) and static difference (SD = SI - IF). The effects of CSN stimulation were also evaluated during changes in the state of intrafusal muscle fibre contraction induced by succinylcholine and curare. In a population of 124 MSAs, 106 units (85.4 %) were affected by sympathetic stimulation. In general, while changes in resting discharge varied among different units (Ia vs. II) and experimental conditions (curarised vs. non-curarised), ranging from enhancement to strong depression of firing, the amplitude of the response to muscle stretches consistently decreased. This was confirmed and detailed in a quantitative analysis performed on 49 muscle spindle afferents. In both the non-curarised (23 units) and curarised (26 units) condition, stimulation of the CSN reduced the response amplitude in terms of DD and SD, but hardly affected DI. The effects were equally present in both Ia and II units; they were shown to be independent from gamma drive and intrafusal muscle tone and not secondary to muscle hypoxia. Sympathetic action on the resting discharge (IF) was less consistent. In the non-curarised condition, IF decreased in most Ia units, while in II units decreases and increases occurred equally often. In the curarised condition, IF in group II units mostly increased. The results have important functional implications on the control of motor function in a state of 'high' sympathetic activity, like excessive stress, as well as in certain pathological conditions such as sympathetically maintained pain.