Dependence of the Achilles tendon reflex on the excitability of spinal reflex pathways

Muscle afferent activity from the triceps surae was recorded during experimentally induced alterations in amplitude of the Achilles tendon jerk. No changes in the neural afferent response to tendon percussion or in the background level of neural activity occurred when the reflex response was altered by discomfort, distraction, changes in attention, or changes in the rate of tendon percussion. Reinforcement of the Achilles tendon jerk by forceful contraction of the forearm muscles did not alter the relationship between intensity of the tendon tap and amplitude of the evoked neural afferent volley. Nevertheless, such maneuvers lowered the reflex threshold and raised reflex sensitivity so that a smaller afferent volley was required to produce a tendon jerk, and an increase in the afferent volley produced a disproportionately greater increase in reflex electromyographic activity than would have occurred at rest. Reinforcement maneuvers potentiated the H-reflex but did not alter the electrically induced afferent volley or the background level of neural activity. It is concluded that these changes in reflex responsiveness occurred through intrinsic spinal mechanisms independent of the fusimotor system.     

Effects of the Jendrassik manoeuvre on muscle spindle activity in man.

Twenty-eight mechanoreceptive units identified as primary or secondary spindle afferents were sampled from muscle nerve fascicles in the median, peroneal, and tibial nerves of healthy adult subjects. The responses of these units to sustained passive muscle stretch, to passive stretching movements, to tendon taps, and electrically-induced muscle twitches were studied while the subject performed repeated Jendrassik manoeuvres involving strong voluntary contractions in distant muscle groups. The manoeuvres had no effect upon the afferent spindle discharges as long as there were no EMG signs of unintentional contractions occurring in the receptor-bearing muscle and no mechanotransducer signs of unintentional positional changes altering the load on that muscle. Unintentional contractions in the receptor-bearing muscle frequently occurred during the manoeuvres, however, and then coactivation of the spindle afferents was observed. Multiunit afferent responses to Achilles tendon taps, led off from tibial nerve fascicles, were in a similar way uninfluenced by the Jendrassik manoeuvres, even when these resulted in marked reinforcement of the calf muscle tendon jerk. The results provide no evidence for fusimotor sensitization of spindles in muscles remaining relaxed during the Jendrassik manoeuvre, and reflex reinforcement occurring without concomitant signs of active tension rise in the muscles tested is presumed to depend upon altered processing of the afferent volleys within the cord.     

Muscle afferent potential (`A-wave'') in the surface electromyogram of a phasic stretch reflex in normal humans

The experiments reported in this paper tested the hypothesis that the afferent potential elicited by a tendon tap in an isometrically recorded phasic stretch reflex can be detected in the surface EMG of normal humans when appropriate techniques are used. These techniques involved (1) training the subjects to relax mentally and physically so that the EMG was silent before and immediately after the diphasic MAP which reflects a highly synchronous discharge of afferent impulses from low threshold muscle stretch receptors after a tendon tap, and (2) using a data retrieval computer to summate stimulus-locked potentials in the EMG over a series of 16 samples using taps of uniform peak force and duration on the Achilles tendon to elicit the tendon jerk in the calf muscles. A discrete, diphasic potential (`A-wave') was recorded from EMG electrodes placed on the surface of the skin over the medial gastrocnemius muscle. The `A-wave' afferent potential had the opposite polarity to the corresponding efferent MAP. Under control conditions of relaxation the `A-wave' had a latency after the onset of the tap of 2 msec, the peak to peak amplitude was of the order of 5 μV and the duration was in the range of 6 to 10 msec. Further experiments were conducted to show that the `A-wave' (1) was not an artefact of the instrumentation used, (2) had a threshold at low intensities of stimulation, and (3) could be reliably augmented by using a Jendrassik manoeuvre compared with the potential observed during control (relaxation) conditions. The results support the conclusion that the `A-wave' emanates from the pool of muscle spindles which discharges impulses along group Ia nerve fibres in response to the phasic stretch stimulus because the primary ending of the spindles is known to initiate the stretch reflex and the spindles can be sensitized by fusimotor impulses so that their threshold is lowered as a result of a Jendrassik manoeuvre. The finding has important implications for the investigation of the fusimotor system in intact man.     

Human muscle afferent responses to tendon taps. 2. Effects of variations in fusimotor bias.

The effect of varying the fusimotor bias on the muscle spindle responses to light tendon taps has been studied in normal human volunteers using surface electrodes at the wrist for recording whole nerve activity. Reinforcement manoeuvres were found to increase the sensitivity of the afferent responses to the mechanical stimulus. Such sensitisation was found to be exhibited more commonly as a decrease in the latency of the peak of the afferent waveform than as an increase in amplitude. Increase in amplitude of the response was seen in cases where the subject was well relaxed and the test muscle quiescent. A change in furimotor drive was also achieved by asking the subjects to close their eyes voluntarily during the test, thus depriving themselves of the visual feedback. The results under these conditions were found to be variable, though showing considerable changes from control recordings. The effect of reinforcement manoeuvres may perhaps result in increasing the dynamic fusimotor drive. Such an effect may be simulated on occluding the blood supply to the test muscle since ischaemia produces an immediate rise in the rate of afferent discharge. The method of recording is suggested as a convenient technique for clinical use.     

Assessment of fusimotor contribution to reflex reinforcement in humans

The contribution of the fusimotor system to reflex reinforcement such as the Jendrassik manoeuvre was investigated by recording single unit activity with tungsten electrodes from muscle spindle afferent nerves in unanaesthetized normal human subjects. Muscle spindle afferent activity was recorded before, during, and after the reinforcement test. When the leg muscles remained relaxed during the Jendrassik manoeuvre, spindle activity recorded in the tibial nerve was accelerated. Also in the median nerve, activity from muscle spindle afferent fibres was increased during a remote contraction of the ipsilateral quadriceps muscle. Comparing the time course of the phasic reflex reinforcement and the muscle spindle facilitation during the remote contraction, a marked after-effect was recorded in both responses. Present results show an increased spontaneous muscle spindle activity in relaxed muscles during a remote muscle contraction, and provide evidence for the contribution of the fusimotor system to the enhancement of phasic reflexes by reinforcement manoeuvres.     

Can neck muscle spindle afferents activate fusimotor neurons of the lower limb?

Introduction: We investigated whether vibratory stimulation of the dorsal neck muscles activates fusimotor neurons of lower limb muscles in relaxed human subjects. Methods: The triceps surae (TS) muscles of seated subjects (n = 15) were conditioned to leave their muscle spindles in either an insensitive (hold‐long) or sensitive (hold‐short) state. A vibrator (80 HZ ) was applied to the dorsal neck muscles for 10 seconds. The tendon jerk was evoked from the right TS immediately before (during) or 5 seconds after (interposed) the offset of vibration. Results: The size of the reflex after hold‐long muscle conditioning and after neck vibration was significantly smaller than the control hold‐short reflex (P < 0.001). However, after hold‐short conditioning, neck vibration significantly increased tendon jerk amplitude, both during (P = 0.001) and interposed (P = 0.026). Conclusion: Dorsal neck vibration increases spinal reflex excitability of the TS in relaxed and seated subjects, but not through fusimotor excitation. Muscle Nerve, 2012     

Myoelectric silence following unopposed passive stretch in normal man.

The response to unopposed passive muscle stretch applied during sustained contraction was studied in normal man. When the subject did not resist the stretching force, the initial response was a brief cessation of EMG activity in the elongated muscle. The myoelectric silence was observed repeatedly in muscles of the upper and lower limbs. The response to passive stretch is discussed in relation to the lengthening reaction and the inverse myotatic reflex. The silent period observed under these experimental conditions is unlikely to be caused by Renshaw inhibition, a pause in spindle afferent discharge, or activity of the group II afferent reflex pathway. Possible mechanisms include autogenetic inhibition and a stretch-evoked decrease of fusimotor activity.     

Reproducibility of tendon jerk reflexes during a voluntary contraction.

OBJECTIVES: The present study explored whether testing tendon jerks during voluntary contraction of the test muscle would improve reproducibility by effectively 'clamping' the excitability of the motoneurone pool at firing threshold. METHODS: Tendon jerk reflexes of soleus, tibialis anterior and vastus lateralis and the soleus H reflex were recorded in 12 healthy subjects at rest and during voluntary contractions of 10-20% of maximum. Recordings were repeated 8-10 times in 5 subjects, in whom reflex symmetry was also determined. RESULTS: Not all tendon jerk reflexes could be recorded at rest, and the variability of latency and amplitude was high. All reflexes could be recorded in each subject during contractions. The latency of tendon jerk reflexes decreased by approximately 2 ms during contractions, but H-reflex latency decreased by only 0.2-0.3 ms. For the tendon jerks, an asymmetry of >3.0 ms at rest and >2.5 ms contracting would be outside 3 SD of the normal mean. In repeat studies, the coefficient of variation of reflex latency was <4% for the tendon jerk. CONCLUSIONS: A voluntary contraction could potentiate the tendon jerk by a number of mechanisms, but the most important is probably enhancement of the excitability of the motoneurone pool. The present techniques should increase the value of tendon reflex testing when assessing possible peripheral nerve, plexus and root disturbances.     

Changes in fusimotor outflow during vibration-induced contraction of triceps surae muscles in decerebrate cats

Changes in fusimotor outflow in medial gastrocnemius and lateral gastrocnemius plus soleus nerves were investigated during vibration-induced contraction of triceps surae muscles in decerebrate cats. A sustained increase in spike occurrence appeared in 33 of 58 investigated neurons, and a decrease in 13. Transient changes of an opposite sign occurred in 19 excited and 6 inhibited fusimotor neurons during the rising phase of reflex muscle contraction. The later changes appeared coincidently with silence in the electromyogram. Thus the discharge of one-third of the examined fusimotor population directed to the triceps surae muscles was modulated parallelly with that of the skeletomotor neurons. It is supposed that the changes in fusimotor spike occurrence during the rising phase of reflex muscle tension are induced mainly by changes in afferent input from muscle spindle primary endings and/or Golgi tendon organs. We could not ascertain whether the different responses (excitation vs inhibition) are related to fusimotor type or to changes in transmission through the reflex pathways. The possible influence of the changes in fusimotor outflow on muscle spindle pause and the silent period in skeletomotor discharge at the beginning of reflex muscle contraction induced by vibration is considered.     

THE SILENT PERIOD IN SPASTIC, RIGID, AND NORMAL SUBJECTS DURING ISOTONIC AND ISOMETRIC MUSCLE CONTRACTIONS

The silent period in the triceps surae muscle has been studied in seven normal subjects, six spastic, and eight Parkinsonian rigid patients by averaging 50 EMG traces from each test. In spastics the mean duration of the silent period was longer than in normals, whereas in Parkinsonian patients it did not differ significantly from normals. The duration of the silent period was independent of large variations in the twitch tension obtained by isometric and isotonic recording of the twitch, suggesting that the active inhibition from the tensionsensitive tendon organs is not the main mechanism behind the prolonged silent period in spastics. This appears primarily to be due to an increased pause in the muscle spindle afferent firing during the twitch. The increased duration of the silent period in spastics is compatible with an increased dynamic fusimotor innervation in spasticity.     

The time-course of bilateral changes in the reflex excitability of relaxed triceps surae muscle in human hemiparetic spasticity

Summary Short, rapid dorsiflexion of the normal human ankle induces a single, synchronised reflex EMG response in the initially relaxed triceps surae muscle (TS). In subjects in whom hemiparesis is present as a result of a unilateral ischaemic cerebral lesion, a reflex EMG response can be elicited on either side with timing identical to that of the normal response. The magnitude of the response in hemiparetic subjects, however, differs from the normal on both the side contralateral and that ipsilateral to the causative lesion. Furthermore, the magnitude of this response varies over the time-course of spasticity. Contralaterally to the lesion, a gradual increase in the magnitude of the response to imposed displacement occurs. One year after stroke, the response has reached a level significantly larger than normal. Changes in the magnitude of the contralateral Achilles tendon jerk reflex EMG are apparent earlier than changes in the response to imposed displacement, with exaggerated tendon jerks already being apparent between 1 and 3 months after stroke. On the side ipsilateral to the lesion, a profound depression of the response to imposed displacement is visible as early as a month after stroke. This depression diminishes over the 1st year, but the response has not even then returned to normal values. These changes are not reflected in the ipsilateral tendon jerk response, which remains normal throughout this period. It is thus concluded that at least two processes are at work in determining the reflex excitability of the TS in hemiparetic humans: firstly, a unilateral increase in excitability at a low spinal level on the side contralateral to the lesions, appearing in the 1st month after stroke and producing the exaggerated tendon jerk response on this side; secondly, a bilateral depression mediated unlike the tendon jerk response, over a predominantly polysynaptic pathway and affecting the response to imposed displacement. This depression appears in the 1st month after stroke and gradually becomes less marked over the following year. On the contralateral side, owing to the increase in excitability at a lower level, this does not appear as a reduction in the magnitude of the response to imposed displacement, but rather is evident in the slower time-course of the development of hyperexcitability in this response, relative to that of the tendon jerk reflex.     

Proprioceptive control of human wrist extensor motor units during an attention-demanding task

The responsiveness of the tonically firing single motor units (SMU) to Ia afferent volleys elicited by either mechanical (T-reflex) or electrical nerve stimulation (H-reflex) was tested in the extensor carpi radialis muscle (ECR) while the subjects were maintaining a steady wrist extension force using visual feedback set either at low or high gain. The aim was to determine whether the proprioceptive control of tonic motoneuronal activity depends on the level of attentiveness required by the behavioural context. The response probability of the SMUs to tendon taps was significantly higher (p<0.0001) and that to electrical nerve stimulation was lower (p<0.001) during the more demanding task. Since these changes in SMU responsiveness were not accompanied by any differences in either the motor unit firing patterns or the mean levels of EMG muscle activity, it can be concluded that there were no attention-related changes in the net excitatory drive to the ECR motoneurons. These results are consistent with the idea that fusimotor sensitization of the muscle spindle may have occurred in the more demanding task: an increase in the mechanical sensitivity of the muscle spindles would certainly account for both the T-reflex facilitation and the H-reflex depression observed. The attention-demanding task therefore seemed to involve an independent fusimotor drive activation process. The results of this study suggest that an adaptation of the fusimotor system occurs in humans, depending on the levels of attention and accuracy required to perform the ongoing motor task, as previously reported to occur in animals.     

About the origin of cerebral somatosensory potentials evoked by Achilles tendon taps in humans

This study examines the effects of ischemic hypoxia and cooling of the leg, muscle contraction and vibration on cerebral potentials evoked by Achilles tendon taps and posterior tibial nerve stimulation to obtain indirect evidence leading to the identification of receptors activated by tendon taps. Experiments performed during ischemia of the leg showed that these receptors lie between the ankle and the knee. Cooling of the leg showed that they are located deep in muscles or bone. Experiments performed during vibration and muscle contraction suggest that muscle stretch receptors provide the afferent input responsible for Achilles tendon tap evoked potentials. All of these experiments point to primary muscle spindles in the proximal gastrocnemius-soleus muscle belly as the main source of afferent input for evoking cerebral potentials to Achilles tendon taps in humans.     

Aftereffects of static or dynamic fusimotor activation on primary afferent discharge.

An analysis is presented of the effects of previous static or dynamic fusimotor activity on various phases of primary afferent discharge before and during ramp stretch of the soleus muscle of anesthetized cat. Short term effects (under 1 sec) following termination of fusimotor activity are generally opposite for static and dynamic fusimotor fibers. Compared to control levels, there is a pronounced depression of primary afferent discharge shortly after termination of static fusimotor activation, and a facilitation following termination of dynamic fusimotor activation. Facilitatory and depressive effects on afferent discharge at periods beyond 1 sec following cessation of fusimotor activation are similar for static and dynamic fusimotor fibers. Possible mechanisms of these changes are discussed in terms of changes in muscle spindle actin-myosin crossbridges, receptor adaptation, and the innervation of nuclear bag and nuclear chain spindle fibers.     

Independence of skeletomotor and fusimotor activity in man?

The activity of human muscle spindle afferents from finger extensor muscles has been studied during voluntary movements in a visual tracking paradigm. With an elastic load the spindle discharge rate was disproportionately high when the opposing force was close to zero, suggesting that the fusimotor drive was high when the direct afferent information about the size of the load that the subject had to handle was poor.     

Tendon areflexia in congenital myopathies accompanied by atrophy of type I fibers. Electrophysiologic study

A predominance and/or an atrophy of type I fibers and a loss of deep tendon reflexes are often observed in different types of congenital myopathy. Various data indicate that both findings can be linked: dysfunction of the myotatic reflex can induce predominant involvement of type I fibers. In order to specify the mechanism of the loss of tendon reflex, an investigation of the Hoffmann reflex (H reflex) was performed in one case of centronuclear myopathy and in one case of congenital type fiber disproportion with type I hypertrophy. The Achilles tendon reflex was absent but the H reflex showed normal recruitment amplitude and latency. The Jendrassik maneuver reinforced the H reflex. These results indicate the involvement of muscle spindles or impairment of the fusimotor system. Nuclear bag intrafusal fibers have common characteristics with type I extrafusal fibers. Both types of fibers could be involved simultaneously in congenital myopathies, thus explaining the loss of tendon reflex.     

The motor tinel sign: a useful sign in entrapment neuropathy?

The motor Tinel sign (MTS) refers to electromyographic activity, sometimes associated with a visible muscle jerk, evoked by percussion or manipulation of a peripheral nerve. The MTS is found in entrapment neuropathies (such as carpal tunnel syndrome or entrapment of the ulnar nerve at the elbow and peroneal nerve at the fibular head) but occasionally also in normal subjects. The MTS may be useful in evaluating patients with entrapment neuropathy, but it does not always indicate nerve dysfunction.     

Attenuated dynamic responses of primary endings of muscle spindles: a basis for depressed tendon responses in acrylamide neuropathy.

Depressed or lost tendon reflexes commonly observed in patients with peripheral neuropathies may result partly from attenuation of the dynamic discharge from the primary endings of muscle spindles. This possibility was investigated in cats with an experimental neuropathy induced with acrylamide (30 mg/kg/day intramuscularly). Achilles tendon reflexes and the dynamic discharge from primary muscle spindles were evaluated after five or ten injections of acrylamide. After five injections the animals were moderately impaired neurologically, the Achilles tendon reflex was difficult to elicit in 2 of 5 animals, and the dynamic responses of primary endings of soleus muscle spindles to stretch were depressed. Following ten injections of acrylamide the cats were severely impaired neurologically; tendon responses were either absent or difficult to elicit, and the dynamic responses of their muscle spindles to stretch were reduced by 50% (p less than 0.01). Additionally, the spindels responded to stretch with only 20 to 30% the normal number of afferent impulses. These data suggest that lost tendon responses in acrylamide neuropathy result in part from inadequate activation of motoneurons by spindle afferent discharge.     

Support stability influences postural responses to muscle vibration in humans

We studied the effect of support stability on postural responses to the vibration of Achilles tendons and of neck dorsal muscles in healthy humans. For this purpose we compared postural responses on a rigid floor and on 6 cm high rocking supports (see-saws) of different curvatures (different radii: 30, 60 and 120 cm). The subject stood with eyes closed, the centre of the feet coincided with the centre of the see-saw. We recorded platform tilt, horizontal displacements of the upper body, ankle joint angle and activity of ankle joint muscles. On the rocking platform subjects maintained balance in a sagittal direction by making see-saw rotations placing the support under the body's centre of gravity. Equilibrium maintenance requires that the torque in the ankle joint increases during forward body displacements, as on the rigid floor, and be accompanied by a plantar flexion (not by a dorsiflexion) in the ankle joint. The directional dependence of vibration-induced reactions on the see-saw was the same (relative to space) as on the rigid floor: backward body displacement during Achilles tendon vibration and forward body displacement during neck muscle vibration. A decrease of support stability (with a decrease of the radius from 120 to 30 cm) diminished significantly the effect of Achilles tendon vibration and to a lesser extent the effect of neck muscle vibration. In contrast, the increase of platform stability by hand contact with a stable external object gave rise to prominent body sway in response to Achilles tendon vibration. Neck muscle vibration on the movable support provoked a quick initial forward body sway. This initial quick response was absent during vibration of the Achilles tendons. We conclude that postural responses to muscle vibration reflect the participation of different muscles in posture control and depend on the support properties. Support instability changes the role of proprioceptive information and the state of the system of equilibrium maintenance.     

Event-related slow potentials evoked during ankle jerk conditioning in wakefulness and NREM sleep

Slow cortical potentials related to the ankle jerk and to its conditioning were studied in 40 adults while awake and during NREM sleep. A weak sound (S) was used as conditioned stimulus, while the ankle jerk, evoked either by Achilles tendon percussion (P) or by electrical stimulation of the sciatic nerve (H), served as unconditioned or 'imperative' stimulus. During waking, responses to simple stimuli (S, P, H) were mostly negative. During S-P and S-H pairs, responses to S were mainly negative, resembling the CNV, while these to P or to H became mostly positive, like the CNV resolution or the positive phase of the motor potential. During NREM sleep, responses to simple as well as to paired stimuli showed mostly a biphasic (negative-positive) morphology resembling the K complex. The conditioned slow potential changes obtained by pairing a sound with the ankle jerk therefore seem to be abolished during NREM sleep. This absence of conditioning can be related to the absence of habituation during NREM sleep. In 35% of the cases, however, positive slow waves were evoked by paired sounds during sleep. The possible significance of these phenomena is discussed.