Lateral rectus whole muscle and motor unit contractile measures with the extraocular muscles intact

Both extracellular and intracellular stimulation of single motoneurons were shown to be similarly effective and consistent in eliciting contractile responses in single lateral rectus muscle motor units. The whole muscle was activated by stimulating the sixth nerve in the brain stem. Both whole muscle and motor unit contractile characteristics, under isometric conditions, were found to remain consistent regardless of whether this extraocular muscle was detached or left attached to the globe. In addition, whole muscle twitch and maximum tetanic tension evoked by sixth nerve stimulation was significantly less than would be predicted by the linear summation of individual motor unit twitch and maximum tetanic tensions.     

Frequency of tendon organ discharges elicited by the contraction of motor units in cat leg muscles

1. The responses elicited in individual tendon organs by the contraction of single motor units were studied in peroneus longus, peroneus brevis, tibialis anterior and soleus muscles. 2. No simple relation was found between the discharge frequency of a tendon organ and the tension produced in the muscle tendon by the contraction of individual motor units. 3. The sensitivity of a given tendon organ to contractile tension was not the same for each of the motor units which elicited its discharge. There was no correlation between the sensitivity of the receptor and the strength of the motor units. 4. Upon repetitive stimulation of a tendon-organ-activating motor unit at increasing rates, the frequency of the receptor sustained discharge reached a maximal value for rates of stimulation eliciting submaximal tetanic tension. Higher rates only produced an increase in the dynamic component of the tendon organ response. 5. These observations show that the contractile tension sensed by a tendon organ is not a simple fraction of the tension which appears at the muscle tendon. They might be accounted for as consequences of the fine structure of tendon organs and of variations in the number of muscle fibres contributed by different motor units to the bundle inserted on each receptor. The location of most tendon organs at musculo-aponeurotic junctions rather than in the tendon proper, could also be responsible for some of the observed discrepancies.     

Spontaneous electromyographic activity in adult rat soleus muscle

Single-motor-unit and gross electromyograms (EMG) were recorded from the soleus muscle in six unrestrained rats. The median firing frequencies of nine motor units were in the 16-25 Hz range, in agreement with previous studies. One additional motor unit had a median firing frequency of 47 Hz. This unit and one of the lower-frequency units regularly fired doublets. Motor-unit firing frequency was well correlated to whole-muscle EMG during locomotion. Integrated rectified gross EMG revealed periods of continuous modulation, phasic high-amplitude events, and tonic low-amplitude segments. The tonic segments typically were caused by a small number of motor units firing at stable high frequencies (20-30 Hz) for extended periods of time without detectable activity in other units. This long-lasting firing in single motor units typically was initiated by transient mass activity, which recruited many units. However, only one or a few units continued firing at a stable high frequency. The tonic firing terminated spontaneously or in conjunction with an episode of mass activity. Different units were active in different tonic segments. Thus there was an apparent dissociation between activity in different single motor units and consequently between single-motor-unit activity and whole-muscle EMG. It is proposed that the maintained tonic motor-unit activity is caused by intrinsic motoneuron properties in the form of depolarizing plateau potentials.     

Summation of extraocular motor unit tensions in the lateral rectus muscle of the cat

Contractile measures on 67 single muscle units in the cat lateral rectus muscle were made in response to motoneuron stimulation. Simultaneous activation of four to five additional units, using muscle nerve stimulation, allowed an examination of unit force summation. Linear force addition was found in 73% of the units, while 25% added only about half of their twitch force to the twitch force of the nerve-activated units. "Nonadditive" units had significantly weaker twitch tensions than the units which added linearly. Lengthening or shortening the whole muscle, from maximal isometric settings, reduced whole muscle twitch tension as well as muscle unit tension. Injury to the lateral rectus muscle did not significantly alter whole muscle tension. These findings suggest that the known serial and branching arrangement of these muscle fibers, as well as the complex interfiber matrix, may help explain the force reduction in some muscle units and the whole muscle's resistance to insult.     

Dissociation of the electrical and contractile properties in single human motor units during fatigue

The surface EMG area often exhibits progressive enlargement during a submaximal fatiguing contraction, but the underlying reasons still remain uncertain. Fatigue-induced changes in the surface-detected motor unit action potentials (S-MUAPs) of 10 human thenar motor units (MUs) with widely differing physiological properties were examined. After 2 min of repetitive 40-Hz stimulation, the size of the S-MUAPs of all MUs increased, the magnitude of which was negatively correlated with their tetanic tension changes. These findings suggest that during muscle fatigue, in addition to reflecting recruitment of new MUs and increases in firing rates of the active MUs, the surface EMG may also be markedly influenced by changes in the S-MUAPs, especially in fast fatigable muscles.     

Adaptations of rat lateral gastrocnemius motor units in response to voluntary running

This study investigated the effects of 12 wk of voluntary wheel running on motor units from rat lateral gastrocnemius. Motor units were isolated via ventral root splitting (L5) from active or sedentary rats and were classified into slow, fast-fatigue-resistant, and fast-fatigable (FF) units. An overall increase in mean motor unit tetanic tension (35%) was accompanied by a decrease in mean motor unit fatigue resistance (-10%). These adaptations were localized in the fast unit population but varied among fast motor unit subtypes. The overall increase in tetanic force was due primarily to increases in fast-fatigue-resistant units (300%), whereas changes in fatigue resistance (-43%) were confined to FF units. However, the changes seen with activity may have been partly obscured by classifying fast motor units based on fatigability, since a significant increase in tetanic force accompanied by a decreased twitch one-half relaxation time was apparent in units falling in the midrange of the tetanic force continuum and included a number of FF units. These data provide direct demonstration of nonuniform motor unit adaptations subsequent to increases in normal functional activity.     

Properties of motor units of the frog sartorius muscle

1. The mechanical properties of single motor units in the sartorius muscle of the frog Litoria aurea were examined during single shock and repetitive stimulation of motor axons. 2. The tetanic tension developed by motor units lay in the range 1-40% of whole muscle tension with two peaks in the distribution, in the range 5-10% and 25-30%. The large units had briefer times-to-peak for the twitch than the small units and were more readily fatigued during prolonged repetitive stimulation. 3. Histological examination of the muscle gave a count of 620 muscle fibres with a diameter range of 28-128 mum. Cholinesterase stained preparations showed that the majority of muscle fibres had several nerve terminals (mean 3, range 1-5). 4. Muscle fibres received their multiple innervation from different axons (polyneuronal) or branches of the same axon (multiterminal). The presence of polyneuronal innervation of muscle fibres was confirmed by a comparison of the tensions when each of a pair of motor units was stimulated alone and when they were stimulated together. The tension excess, or overlap, was up to 60% when expressed in terms of the tension developed by either unit alone. Motor units developing similar amounts of tension tended to show more overlap in their innervation than units with very different tensions. 5. An estimate of the amount of multiterminal innervation gave variable results but could account for up to 60% of a motor unit's tension. No correlation could be detected between the values for multiterminal innervation and any other measured parameter. However, it is argued that because of the limitations of the measurements the existence of a relationship between the extent of multiterminal or polyneuronal innervation and the mechanical properties of the motor unit cannot be excluded.     

Motor-unit recruitment in self-reinnervated muscle

1. Recruitment order of motor units in self-reinnervated medial gastrocnemius (MG) muscles was studied in decerebrate cats 16 mo after surgical reunion of the cut MG nerve. Pairs of MG motor units were isolated by dual microelectrode penetration of ventral roots to measure their recruitment sequence during cutaneous reflexes in relation to their physiological properties. 2. Physiological properties of reconstituted motor units appeared normal, as expected. Also normal were the relationships among these properties: twitch and tetanic tension tended to increase with axonal conduction velocity and decrease with twitch contraction time. A small fraction of motor units (10/116) in reinnervated muscles produced either no measurable tension or unusually large amounts of tension compared with controls. This was the only distinct feature of the sample of reconstituted units. 3. In muscles reinnervated after nerve section, stretch was notably ineffective in eliciting reflex contraction of MG muscles or their constituent motor units (only 5/116 units). Incomplete recovery from nerve section was probably the cause of this impairment, because stretch reflexes were readily evoked in adjacent untreated muscles and in one reinnervated MG muscle that was studied 16 mo after nerve crush. In contrast with the ineffectiveness of muscle stretch, sural nerve stimulation succeeded in recruiting 49/116 units, a proportion fairly typical of normal MG muscles. 4. The contractions of the first unit recruited in cutaneous reflexes tended to be slower and less forceful than those of the other unit in a pair. By these measures, recruitment obeyed the size principle. This recruitment order with respect to unit contractile properties was not significantly different (P > 0.05) between untreated and reinnervated muscles but was significantly (P < 0.005) different from random order in both groups. The same recruitment pattern was observed for pairs of motor units sampled from the muscle reinnervated after nerve crush, whether units were recruited by muscle stretch or sural nerve stimulation. 5. The usual tendency for motor units with slower conduction velocity (CV) to be recruited in sural nerve reflexes before those with faster CV was not strong in reinnervated muscles. After nerve section the proportion of units exhibiting the usual recruitment pattern was not significantly different (P > 0.05) from a random pattern for CV. 6. The central finding is that the normal recruitment patterns recover from nerve injury in a muscle that is reinnervated by its original nerve. By contrast, stretch reflexes do not recover well from nerve section, and this deficiency may contribute to motor disability.     

Properties of motor units after immobilization of cat peroneus longus muscle

Changes in contractile properties of cat peroneus longus motor units were studied 2, 5, and 8 wk after selective immobilization of this muscle, which was achieved by fixing the distal tendon of the peroneus longus to the fibula either at the muscle minimal physiological length ("short" length) or at the length for a 90 degree ankle joint ("neutral" length). In each muscle, 75-90% of the units [slow (S), fast resistant to fatigue (FR), fast intermediate (FI), and fast fatigable (FF)] were studied. Immobilization elicited a permanent decrease in tetanic force developed by single motor units, which was larger for resistant-to-fatigue units (S, FR). In most instances this decrease was not related to the immobilization length. In all units, twitch contraction and half-relaxation times underwent a transient increase, the extent and time course of which were influenced by immobilization length. The relationship between the frequency of motor units activation and the ratio of unfused to maximal tetanic force was studied. For fast units, there was a transient shift of the relation toward low frequencies after 2 and 5 wk of immobilization at neutral and short length, respectively.     

Rank-ordered regulation of motor units

Myoelectric signals were detected from the tibialis anterior muscle of 5 subjects with a quadrifilar needle electrode while the subjects generated isometric forces that increased linearly with time (10% of maximal voluntary contraction/s) up to maximal voluntary level. Motor unit firing rates were studied as a function of force throughout the full range of muscle force output. The relationship between force and firing rate was found to contain three distinct regions. At recruitment and near maximal force levels, firing rates increased more rapidly with force than in the intermediate region. Furthermore, in the regions with rapid increases, the rate of change of firing rate was correlated to the recruitment threshold, with higher recruitment threshold motor units displaying greater rates of change. In the intermediate region, all motor units had similar rates of change of firing rate. A weak positive correlation was found between initial firing rate and recruitment threshold. Firing rates of motor units at any instant were found to be ordered according to the recruitment order: at any given time in the contraction motor units with lower recruitment thresholds had higher firing rates than units with higher recruitment thresholds. Firing rates of all motor units were observed to converge to the same value at maximal forces. Mechanisms underlying motor unit recruitment and firing rate modulation are discussed in the context of a conceptual model.     

Fast-to-slow conversion following chronic low-frequency activation of medial gastrocnemius muscle in cats. I. Muscle and motor unit properties

This study of cat medial gastrocnemius (MG) muscle and motor unit (MU) properties tests the hypothesis that the normal ranges of MU contractile force, endurance, and speed are directly associated with the amount of neuromuscular activity normally experienced by each MU. We synchronously activated all MUs in the MG muscle with the same activity (20 Hz in a 50% duty cycle) and asked whether conversion of whole muscle contractile properties is associated with loss of the normal heterogeneity in MU properties. Chronically implanted cuff electrodes on the nerve to MG muscle were used for 24-h/day stimulation and for monitoring progressive changes in contractile force, endurance, and speed by periodic recording of maximal isometric twitch and tetanic contractions under halothane anesthesia. Chronic low-frequency stimulation slowed muscle contractions and made them weaker, and increased muscle endurance. The most rapid and least variable response to stimulation was a decline in force output of the muscle and constituent MUs. Fatigue resistance increased more slowly, whereas the increase in time to peak force varied most widely between animals and occurred with a longer time course than either force or endurance. Changes in contractile force, endurance, and speed of the whole MG muscle accurately reflected changes in the properties of the constituent MUs both in extent and time course. Normally there is a 100-fold range in tetanic force and a 10-fold range in fatigue indexes and twitch time to peak force. After chronic stimulation, the range in these properties was significantly reduced and, even in MU samples from single animals, the range was shown to correspond with the slow (type S) MUs of the normal MG. In no case was the range reduced to less than the type S range. The same results were obtained when the same chronic stimulation pattern of 20 Hz/50% duty cycle was imposed on paralyzed muscles after hemisection and unilateral deafferentation. The findings that the properties of MUs still varied within the normal range of type S MUs and were still heterogeneous despite a decline in the variance in any one property indicate that the neuromuscular activity can account only in part for the wide range of muscle properties. It is concluded that the normal range of properties within MU types reflects an intrinsic regulation of properties in the multinucleated muscle fibers.     

The influence of the graft length on the functional and morphological result after nerve grafting: an experimental study in rabbits

Clinical experience shows that the results after the use of long nerve grafts for reconstruction are sometimes poor. Nevertheless several authors have stressed that the concomitant big defect in the soft tissues necessitating the use of long grafts is the reason for some of the failures.In 22 rabbits the saphenous nerve was used as a nerve graft. Animals were separated into 3 groups with different lengths of the grafts, namely 3 cm (group 1), 5 cm (group 2) and 7 cm (group 3). In the left hindlimb the proximal end of the graft was coapted to the cut motor nerve branch of vastus medialis. In a second stage the distal end of the graft was coapted to the nerve branch of rectus femoris. After a total period of 15 months the maximum tetanic tension in the reinnervated rectus femoris and in the contralateral unoperated muscle was determined. Biopsies of the graft and the motor branch distal to the graft were taken in order to count the number of regenerated myelinated nerve fibers.The average maximum tetanic tension in the rectus femoris muscle reinnervated by the 3 cm long graft was 27.2 N, in group 2 the force was 20.5 N. In group 3 the maximum force was 17.6 N, which meant an average loss of 29% compared to the contralateral unoperated muscle. The mean number of regenerated myelinated fibres distal to the graft in the rectus femoris motor branch was 1683 in group 1 and decreased to 1137 in group 3.The results show that the length of the graft influences the results after nerve grafting to a certain extent, but a combination of other factors like concomitant soft tissue injury and destroyed target organs may also be responsible for some of the poor results after the clinical use of long nerve grafts.     

Fixation of spinal reflex alterations in spinal rats by sensory nerve stimulation.

Two preparations in which sensory nerve stimulation was used to obtain peripherally induced spinal fixation in spinal rats are described. In the first preparation, proportionally greater amounts of persisting poststimulation flexor muscle contraction, as measured by a force displacement transducer, were produced as stimulation time was increased from 10 min to 40 min. In the second preparation, sensory nerve stimulation was delivered, and evoked whole-nerve responses were recorded from a flexor motor nerve. Results indicated that 30 min or more of sensory nerve stimulation produced increases in response amplitude and area that persisted for at least 30 min after stimulation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Heteronymous H-reflex in temporal muscle motor units

An electric stimulation of the masseteric nerve elicits a heteronymous H-reflex in the temporal muscle. The characteristics of this reflex response were investigated by analysis of the firing probability changes of single motor units. Eleven healthy subjects participated in the experiments. The heteronymous H-reflex of the temporal muscle was electrically elicited by stimulation of the masseteric nerve at 120% of the intensity needed for the maximal masseteric M-wave. From 8 to 24 motor units were sampled from the temporal muscle of each subject. Peri-stimulus time histograms of motor unit recordings were built with a 0.5-ms bin width. The mean firing probability was calculated for the 20 ms preceding the stimulus. The firing probability was considered increased when it exceeded the mean by 3 standard deviations. Of 104 sampled motor units, 40 motor units showed a significant increase of the firing probability, which lasted 1 ms or less in 29 of them. In 12 out of 16 motor units, a significant increase of firing probability also persisted at a lower stimulation intensity (120% of the threshold needed to elicit a masseteric M wave). These data indicate that: (1) some temporal muscle motor units are modulated by afferents from the masseter muscle, (2) the heteronymous H-reflex has a monosynaptic component, and (3) there might be a more complex than just monosynaptic organization serving the heteronymous temporal H-reflex. For the latter conclusion regarding synaptic wiring, however, PSTH studies like the present one can offer only indirect evidence, and this question could be better studied in animals.     

Effects of CO2-induced acidification on the fatigue resistance of single mouse muscle fibers at 28 degrees C

The role of reduced muscle pH in the development of skeletal muscle fatigue is unclear. This study investigated the effects of lowering skeletal muscle intracellular pH by exposure to 30% CO2 on the number of isometric tetani needed to induce significant fatigue. Isolated single mouse muscle fibers were stimulated repetitively at intervals of 4-2.5 s by using 80-Hz, 400-ms tetani at 28 degrees C in Tyrode solution bubbled with either 5 or 30% CO2. Stimulation continued until tetanic force had fallen to 40% of the initial value. Exposure to 30% CO2 caused a significant fall in intracellular pH of approximately 0.3 pH unit but did not cause any significant changes in initial peak tetanic force. During the course of repetitive stimulation, intracellular pH fell by approximately 0.3 pH unit in both normal and acidified fibers. The number of tetani needed to reduce force to 40% of the initial value was not significantly different in 5 and 30% CO2 Tyrode. The sole effect of acidosis was to reduce the rate of relaxation of force, especially in fatigued fibers. It is concluded that, at 28 degrees C, acidosis per se does not accelerate the development of fatigue during repeated tetanic stimulation of isolated mouse skeletal muscle fibers.     

Motor units within the normal rat medial gastrocnemius

The contractile properties, fatiguability and axonal conduction velocity were determined for 118 motor units in the medial gastrocnemius of eighteen rats. Fast-twitch and slow-twitch units could be categorized on the basis of the 'sag' test. For the purposes of statistical comparison the fast-twitch units were classified on the basis of their fatiguability as fast-fatiguable (FF), fast intermediate (FI) and fast fatigue-resistant (FR). As such, FR units tended to have a longer isometric twitch time course than other fast-twitch units. On the basis of peak tetanic force FF units were largest (mean 341 +/- 120 mN) followed by FI (145 +/- 85 mN), FR (87.3 +/- 38) and slow units (40.4 +/- 11.0 mN). There were no differences in motor axonal conduction velocity. Although units were categorized, it is clear that for all characteristics investigated the fast-twitch units exist as a continuum. Some of the largest FF units (peak force 350-500 mN) failed to maintain force with high-frequency stimulation (300 Hz) and this was associated with a failure of the EMG signal.     

Effects of botulinum neurotoxin type A on abducens motoneurons in the cat: alterations of the discharge pattern

The discharge characteristics that abducens motoneurons exhibit after paralysis of the lateral rectus muscle with botulinum neurotoxin type A were studied in the alert cat. Antidromically identified motoneurons were recorded during both spontaneous and vestibularly induced eye movements. A single injection of 0.3 ng/kg produced a complete paralysis of the lateral rectus muscle lasting for about 12-15 days, whereas after 3 ng/kg the paralysis was still complete at the longest time checked, three months. Motoneurons recorded under the effect of the low dose showed differences in their sensitivities to both eye position and velocity according to the direction of the previous and ongoing movements, respectively. These directional differences could be explained by post-saccadic adaptation of the non-injected eye in the appropriate direction for reducing ocular misalignment. Thus, backward and forward post-saccadic drifts accompanied on- and off-directed saccades, respectively. The magnitude of the drift was similar to the magnitude of changes in eye position sensitivity. The discharge of the high-dose-treated motoneurons could be described in a three-stage sequence. During the initial 10-12 days, motoneuronal discharge resembled the effects of axotomy, particularly in the loss of tonic signals and the presence of exponential-like decay of firing after saccades. In this stage, the conduction velocity of abducens motoneurons was reduced by 21.4%. The second stage was characterized by an overall reduction in firing rate towards a tonic firing at 15-70 spikes/s. Motoneurons remained almost unmodulated for all types of eye movement and thus eye position and velocity sensitivities were significantly reduced. Tonic firing ceased only when the animal became drowsy, but was restored by alerting stimuli. In addition, the inhibition of firing for off-directed saccades was more affected than the burst excitation during on-directed saccades, since in many cells pauses were almost negligible. These alterations could not be explained by adaptational changes in the movement of the non-injected eye. Finally, after 60 days the initial stages of recovery were observed. The present results indicate that the high dose of botulinum neurotoxin produces effects on the motoneuron not attributable to the functional disconnection alone, but to a direct effect of the neurotoxin in the motoneuron and/or its synaptic inputs.     

Discharge pattern of single motor units in the tonic vibration reflex of human triceps surae

Using a single fibre EMG electrode the firing pattern of 46 motor units in the triceps surae has been studied during vibration of the Achilles tendon at frequencies of 25--200 Hz. Potentials activated in the tonic vibration reflex (TVR) were phase-locked to the vibration cycle but tended to become somewhat less so with continued vibration. The firing pattern of voluntarily activated motor units became locked to the waveform by the application of the vibrator. The discharges of 21 motor units were studied during low threshold (sub-M wave) tetanic stimulation of the tibial nerve at 25--100 Hz. No evidence was found of synchronization of potentials activated in the resulting tonic contraction. During weak voluntary contractions, stimulation also failed to regularize voluntarily activated motor units. The findings can be reconciled by postulating that, in normal man, vibration activates monosynaptic and polysynaptic pathways, the latter circuit being adequate to generate reflex contraction, while the former merely affects the temporal patterning of the motor outflow.     

Premotor commands encode monocular eye movements

Binocular coordination of eye movements is essential for stereopsis (depth perception) and to prevent double vision. More than a century ago, Hering and Helmholtz debated the neural basis of binocular coordination. Helmholtz believed that each eye is controlled independently and that binocular coordination is learned. Hering believed that both eyes are innervated by common command signals that yoke the eye movements (Hering's law of equal innervation). Here we provide evidence that Hering's law is unlikely to be correct. We show that premotor neurons in the paramedian pontine reticular formation that were thought to encode conjugate velocity commands for saccades (rapid eye movements) actually encode monocular commands for either right or left eye saccades. However, 66% of the abducens motor neurons, which innervate the ipsilateral lateral rectus muscle, fire as a result of movements of either eye. The distribution of sensitivity to ipsilateral and contralateral eye movements across the abducens motor neuron pool may provide a basis for learning binocular coordination in infancy and adapting it throughout life.     

Responses of Purkinje cells of cerebellar vermis to sinusoidal rotation of neck

1. The response of Purkinje (P) cells located in the vermal cortex of the cerebellar anterior lobe to sinusoidal rotation of the neck was investigated in precollicular decerebrate cats. The head of the animal was fixed in a sterotaxic frame while the spinous process of the second cervical vertebra was held by a clamp rigidly fixed to the tilting table. It was then possible to elicit a selective neck input by rotating the neck and the body simultaneously along the longitudinal axis of the animal while maintaining the head in horizontal position. 2. Among the 95 P-cells tested for neck stimulation, 35 units showed a mossy fiber (MF) or a climbing fiber (CF) response to sinusoidal rotation of the axis vertebra at the frequency of 0.026 Hz and at the peak amplitude of displacement of 5--10 degrees. The response consisted in a periodic modulation of the discharge frequency during sinusoidal rotation of the neck. Most of these units were excited during side-down rotation of the neck, but were inhibited during side-up rotation. 3. The threshold amplitude of neck rotation responsible for the MF-induced responses varied in different units from 1 to 3 degrees at the frequency of 0.026 Hz. The sensitivity of the units, expressed in percentage change of the average firing rate per degree of displacement, either did not change or very slightly decreased as a result of increasing amplitude of stimulation from 1--3 degrees to 10--15 degrees at the frequency of 0.026 Hz or by increasing frequency of neck rotation from 0.015 to 0.15 Hz at the amplitude of neck displacement of 5--10 degrees. 4. Changes in amplitude or frequency of stimulation at the parameters reported above did not greatly modify the phase of the unit responses relative to the side-down position of the neck. These findings indicate that the MF and CF responses of P-cells to sinusoidal rotation of the neck depended on changes in neck position and not on changes in velocity of neck rotation. 5. The observation that the majority of responding P-cells located in the vermal cortex of the cerebellar anterior lobe increased their firing rate during side-down rotation of the neck is discussed in relation to the results of stimulation and lesion experiments, indicating that postural changes can be elicited either during asymmetric stimulation of neck receptors or by unilateral interruption of the neck afferents.