Stretch reflex variation in the relaxed and the pre-activated quadriceps muscle of normal humans

The stretch reflex to patellar tendon taps was quantified by force measurements at the ankle in 7 normal subjects. In each experiment the stretch reflex was elicited from 14 consecutive stretches by two types of hammers (an ordinary hand-held hammer and a motorized hammer) in the relaxed and the pre-activated quadriceps muscle. The coefficient of variation for the 14 stretch reflexes fell from 54% in the relaxed muscle to 39% in the contracting muscle (p less than 0.05). The stretch reflex varied less between the different levels of active contraction than between the relaxed state and the contracted level (p less than 0.05). The experiment was repeated in all subjects and at all contraction levels. The coefficient of variation of the mean for the two experiments fell non-significantly from a mean value of 27% in the relaxed muscle to 14% in the contracting muscle. The coefficients of variation for the two hammers were almost identical. It is concluded that quantification of the stretch reflex can be made more precisely in the contracting muscle.     

TVR and vibration-induced timing of motor impulses in the human jaw elevator muscles.

In order to investigate myotatic reflex involvement in jaw muscle control, an analysis was made of the motor responses induced by mechanical vibration (120-160 Hz) of the jaw elevator muscles in healthy subjects. As seen in torque measurements and mean-voltage electromyographic (EMG) recordings, the vibration caused involuntary reciprocal changes in jaw muscle tone, the contraction force increasing in jaw elevators and decreasing in antagonistic jaw opening muscles. This tonic vibration reflex (TVR) elicited from the jaw elevators exhibited many characteristics similar to those previously described for limb muscle tonic vibration reflexes: it varied in strength from one subject to the next independently of the briskness of the jaw elevator tendon jerks; it had a gradual onset with successive recruitment of jaw elevator motor units firing largely out of phase with one another and at rates much lower than the vibration frequency; it was susceptible to voluntary control--when allowed visual feed-back from the torque meter all subjects were able to suppress the TVR and keep mean contraction force constant. The results indicate that with respect to the tonic motor response to sustained inflow in the Ia afferent nerve fibres, the jaw elevators do not differ markedly from other skeletal muscles. Independently of whether a TVR was present or not, the vibration caused a timing of the motor unit discharges in the jaw elevators that could not be controlled voluntarily and that showed up in gross EMG recordings as a marked grouping of discharges synchronous with each wave of vibration. A similar but less distinct grouping of the gross EMG pattern was seen in limb muscles exposed to vibration, the dispersion increasing with the peripheral conduction distances of the reflex arcs. It is suggested that contrary to the TVR, which depends on the sustained mean level of the Ia afferent input, the timing phenomenon depends, like the tendon jerk, on the degree of synchrony in the afferent Ia volleys. Monosynaptic projections may well be involved in the dynamic timing of motor discharges during tonic firing, but this does not imply that the TVR or the tonic stretch reflex is dependent upon such projections.     

Effect of contraction level and magnitude of stretch on tonic stretch reflex transmission characteristics.

Electromyogram tonic stretch reflex responses were recorded from biceps brachii muscles in normal and cerebral palsied subjects sustaining either 10% or 20% of maximum voluntary contraction and attempting to keep the elbow stiff in a fixed position. The muscle was stretch by a sinusoidal perturbation applied by the experimenter to the elbow angle. Five different amplitudes of stretch were employed ranging 1.67 to 10.0 degrees peak to peak variation of elbow angle. Spectral analysis of the rectified and filtered electromyogram revealed "noisy" sinusoidal reflex responses with negligible harmonic distortion but the amplitude of the reflex responses did not increase linearly with the amplitude of stretch. An analysis of variance showed that for both groups of subjects the gain of the tonic stretch reflex increased significantly (p less than 0.001) with contraction level and decreased significantly (p less than 0.001) with magnitude of stretch. This finding illustrates that both magnitude of stretch and level of contraction need to be carefully controlled when measures of tonic stretch reflex responses are used to assess changes of muscle tone.     

Stretch reflexes of triceps surae in normal man.

In order to learn more about stretch reflex behaviour of triceps surae, normal human subjects sat in a chair with one foot on a platform attached to a torque motor that produced phasic dorsiflexion displacements on the ankle. EMG activity was recorded from triceps surae and responses were obtained for various conditions. When the subjects's foot was relaxed, stretch of triceps surae produced a single EMG component at short-latency which increased in magnitude with increasing velocity of stretch. The response was not altered if the subject was asked to plantarflex or dorsiflex the ankle voluntarily when he felt the perturbation. It was reduced by vibration of the Achilles tendon. If the triceps surae was stretched while the subject plantarflexed his ankle, the short-latency response was followed by one and sometimes two long-latency responses. Like the short-latency reflex when the foot was relaxed, none of these responses was altered by the subject's planned movement after feeling the perturbation. All of the responses were suppressed to a similar degree by vibration. The long-latency reflexes depended on long-duration of stretching and relatively slow acceleration of stretch. The reflexes persisted after anaesthesia to the foot suggesting that muscle afferents were responsible. Interactions between H-reflexes and stretch-reflexes revealed that the afferent volley producing a stretch reflex acted like the afferent volley producing a small H-reflex. Responses at an interval of 30 ms to both an electrical stimulus for an H-reflex and a stretch stimulus were possible if the electrical stimulus produced only a small H-reflex and if the subject had been plantarflexing the ankle. The short-latency reflex when the foot was relaxed or exerting a background force appears to be the monosynaptic, Ia mediated stretch reflex. The physiological properties of the long latency reflexes are similar to those of the short-latency reflex, and they may represent, at least to a certain extent, response of the motor neuron pool to successive Ia bursts.     

Physiological mechanisms of rigidity in Parkinson''s disease.

Electromyographic responses of triceps surae and tibialis anterior produced by dorsiflexion stretch were studied in 17 patients with Parkinson's disease. Most patients showed increased muscular activity when attempting to relax. A few patients showed an increase of short-latency reflexes when relaxed and when exerting a voluntary plantarflexion prior to the stretch. Many patients showed long-latency reflexes when relaxed and all but one showed long-latency reflexes with voluntary contraction; and these reflexes were often larger in magnitude and longer in duration than those seen in normal subjects. Unlike the short-latency reflex, the long-latency reflex did not disappear with vibration applied to the Achilles tendon. The long-latency reflexes and continuous responses to slow ramp stretches were diminished at a latency similar to the beginning of long-latency reflexes when the stretching was quickly reversed. Dorsiflexion stretch also frequently produced a shortening reaction in tibialis anterior. Of all the abnormal behavior exhibited by the Parkinsonian patients only the long-latency reflex magnitude and duration correlated with the clinical impression of increased tone. The mechanism of the long-latency reflex to stretch which is responsible for rigidity is not certain, but the present results are consistent with a group II mediated tonic response.     

Effect of vibration of the ankle stretch reflex in man

Vibration at frequencies above 50 Hz applied to the tendon of the extensor muscles of the ankle joint produce the tonic vibration reflex (TVR) which increases when the vibration frequency is increased. The TVR affects a joint's mechanical response to sinusoidal and random oscillations in a manner similar to that seen with tonic voluntary contraction. Although the myotatic reflex is suppressed by vibration, repeated stretches of sinusoidal oscillation produce an average EMG response which is not different in magnitude from the no vibration case. Either polysynaptic mechanisms at the spinal cord level of mechanisms involving higher centers (and possibly both) are able to overcome the inhibitory mechanisms at the Ia-alpha motoneuron level in producing a stretch evoked resonance near 6 Hz. The degree of inhibition of the myotatic component of the stretch reflex is proportional to the vibration frequency. This is in contrast to the facilitation of the myotatic reflex produced by tonic voluntary contraction. Vibration does not seem to influence the post-myotatic component (> 100 msec) of the stretch reflex. These results indicate that the post-myotatic responses to limb perturbation are not only different in their latency but also in their functional dependence upon peripheral influences.     

Triceps surae fascicle stretch is poorly correlated with short latency stretch reflex size

Introduction: The short latency stretch reflex (SLR) is well described, but the stimulus that evokes the SLR remains elusive. One hypothesis states that reflex size is proportional to muscle fiber stretch, so in this study we examined the relationship between these 2 parameters in human triceps surae muscles. Methods: Achilles tendon taps and dorsiflexion stretches with different amplitudes and preactivation torques were applied to 6 participants while electromyography and muscle fascicle length changes were recorded in soleus and medial gastrocnemius (MG). Results: In response to tendon taps, neither fascicle length nor velocity changes were correlated with SLR size in either muscle, but accelerometer peaks were observed immediately after hammer–tendon contact. Similar results were obtained after dorsiflexion stretches. Conclusion: Muscle fascicle stretch is poorly correlated with SLR size, regardless of perturbation parameters. We attribute the SLR trigger to the transmission of vibration through the lower limb, rather than muscle fiber stretch. Muscle Nerve 52 : 245–251, 2015     

Comparison of spinal myotatic reflexes in human adults investigated with cross-correlation and signal averaging methods

A cross-correlation method for recording spinal myotatic reflexes has been developed to meet the need for brief test periods in babies and children and subjects with central neurological pathology. In normal adult subjects the method has been validated by comparing excitatory and inhibitory reflexes obtained with cross-correlation with those obtained with conventional signal averaging. In the cross-correlation method a pseudo-random binary sequence of 64 brief tendon taps was delivered in <1.5 s, and in the averaging method 20-150 taps at one per second. The reflexes were expressed as unit impulse responses to enable direct, quantitative comparisons to be made. With cross-correlation the responses were slightly expanded in time, had lower peak amplitudes, and onset latencies advanced by 10 ms, the clock period of the pseudo-random binary sequence. The amplitude of biceps phasic stretch reflex increased with muscle contraction in a similar manner with both methods. In tests for stationarity the amplitude of biceps phasic stretch reflex varied <10% in the first six repeats of the pseudo-random binary sequence. The tap force required at threshold for cross-correlation was approximately half that for averaging, but with both methods the magnitude of biceps phasic stretch reflex varied linearly with tap force over the range of one to two times threshold. The validity of responses obtained with cross-correlation was assessed by a statistical procedure. In conclusion, the cross-correlation method is robust and gives similar results to those obtained with averaging.     

Interaction between voluntary contraction and tonic stretch reflex transmission in normal and spastic patients

Transmission characteristics of tonic stretch reflex (TSR) pathways in both normal and spastic patients have been measured during different levels of sustained voluntary contraction of the biceps brachii muscle. A cross-correlation technique of analysis was used to separate reflex responses from the total electromyographic activity. TSR transmission in normal subjects was observed to change with the level of voluntary contraction; sensitivity to stretch increased approximately three-fold as the subject stiffened the arm by simultaneously contracting flexor and extensor muscles. In contrast, TSR transmission did not alter during voluntary contraction in spastic patients. It is proposed that in spastic patients supraspinal modulation of reflex transmission is impaired because hypersensitive spinal reflexes short-circuit long loop pathways.     

A physiological approach to motor disorders.

Spasticity in man is presented as a disinhibition of spinal cord mechanisms, the responses to stretch depending on the interaction of the reflex effects of group Ia with those of group II afferent fibres. The reflex responses to muscle stretch and shortening in Parkinson's disease do not depend on an abnormality of spinal reflex mechanisms. The superimposition of physiological tremor or alternating tremor in rigidity produces the classical cog-wheel sensation. The phase lead of the action tonic stretch reflex was found to be reduced in patients with athetosis and cerebellar disease, thus diminishing damping of unwanted movements. The more complex transmission characteristics of the action tonic stretch reflex of normal man are absent in patients with spasticity and cerebellar lesions, presumably due to interference with long-loop pathways. In normal subjects gain of the reflex loop increases with voluntary contraction but in spasticity gain remains high irrespective of contraction level.     

The limitations of the tendon jerk as a marker of pathological stretch reflex activity in human spasticity.

The motor disorders associated with human spasticity arise, partly from a pathological increase in the excitability of muscle stretch reflexes. In clinical practice, reflex excitability is commonly assessed by grading the reflex response to a blow delivered to the tendon of a muscle. This is a much simpler response than the complex patterns of activity which may be elicited following muscle stretch caused by active or passive movement. Changes in the biceps brachii tendon jerk response have been followed over the first year after stroke in a group of hemiparetic patients and compared with changes in short and medium latency reflex responses elicited by imposed elbow flexion of initially relaxed spastic muscle and with the development of the late reflex responses which contribute to spastic hypertonia. A progressive increase in tendon jerk responses occurred over the first year following stroke, whereas reflex responses to imposed displacement, in particular the late reflex responses contributing to muscle hypertonia, reached their peak excitability one to three months after stroke, with a subsequent reduction in activity. The tendon jerk reflex therefore provides an incomplete picture of the pathological changes in the reflex responses in spasticity.     

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.     

The relationship of voluntary movement to spasticity in the upper motor neuron syndrome

Hyperactive strethch reflexes in the upper motor neuron (UMN) syndrome are frequently cited as an impediment to volitional movement. The assumption is that neural or mechanical activity of the hyperactive antagonist interferes with agonist function. The validity of this assumption was examined by evaluating quantitative and qualitative relationships between stretch reflexes and voluntary movement. Sixteen patients with chronic UMN symptoms and 8 normal volunteers were tested. Joint position and integrated electromyograms from primary flexors and extensors were recorded. Quantitated values of (1) reflex response to controlled passive motion by an automated system, (2) a maximal voluntary isometric contraction, and (3) the time required for ten voluntary rapid repetitive movements (RRM) of alternating elbow flexion and extension were obtained. Passive movement elicited tonic reflexes, which predominated during muscle stretch in patients and during muscle shortening in the volunteers. Ratios of the EMG activity elicited during stretch, shortening, and isometric activity were used as measures of spasticity and were compared with the time for RRM. A positive correlation between elbow flexor spasticity and the time for RRM was shown. Qualitative analysis of the EMG activity during voluntary isotonic movement, however, showed that primary impairment of movement is not due to antagonist stretch reflexes, but rather to limited and prolonged recruitment of agonist contraction and delayed cessation of agonist contraction at the termination of movement.     

Does spasticity contribute to walking dysfunction after stroke?

OBJECTIVES—Clinically, it is assumed thatspasticity of the calf muscles interferes with walking after stroke.The aim was to examine this assumption by evaluating the contributionof spasticity in the gastrocnemius muscle to walking dysfunction in anambulant stroke population several months after stroke.
METHODS—Fourteen stroke patients who were able towalk independently and 15 neurologically normal control subjects wererecruited. Both resting and action stretch reflexes of thegastrocnemius muscle were investigated under conditions that simulatedwalking. Resting tonic stretch reflexes were measured to assessspasticity whereas action tonic stretch reflexes were measured toassess the possible contribution of spasticity to gait dysfunction.
RESULTS—Two thirds of the stroke patientsexhibited resting tonic stretch reflexes which indicate spasticity,whereas none of the control subjects did. However, the stroke patientsexhibited action tonic stretch reflexes that were of similar magnitudeto the control subjects, suggesting that their reflex activity duringwalking was not different from that of control subjects. Furthermore, there was no evidence that the action stretch reflex in the stroke patients contributed a higher resistance to stretch than the control subjects.
CONCLUSIONS—Whereas most of the stroke patientsexhibited spasticity when measured both clinically and physiologically,they did not exhibit an increase in resistance to dorsiflexion due toexaggerated action tonic stretch reflexes. It is concluded that it isunlikely that spasticity causes problems in walking after stroke inambulant patients. Therefore, it seems inappropriate to routinelyreduce or inhibit the reflex response to improve functional movement instroke rehabilitation. Factors other than spasticity should beconsidered when analysing walking after stroke, so that appropriate treatment is provided to patients.

     

Characteristics of the vibratory reflex in humans with reduced suprasegmental influence due to spinal cord injury

The tonic stretch reflex elicited by vibration of a muscle or tendon provides a means of studying segmental reflex activity in humans with impaired volitional motor activity due to spinal cord injury (SCI). Vibration applied to the achilles or patellar tendon in a group of 51 SCI subjects elicited motor unit activity different from that found in 12 healthy subjects. Four distinct features of motor unit responses to vibration of a single tendon (achilles or patellar) could be seen in the SCI subjects: (i) a rapid onset, tonic response, frequently beginning with a single burst analogous to a tendon jerk, in 72% of vibrated sites; (ii) repetitive, phasic bursts of activity or vibratory-induced clonus in 23% of the tonic responses; (iii) spread of activity to muscles distant from the vibration in 44% of the tonic responses; and vibratory-induced withdrawal reflexes (VWR) which occurred after vibration of 37% of the sites. Overall, 81% of stimulated sites responded to vibration in SCI subjects. In contrast, only 54% of vibrated sites responded in control subjects, always with a gradual onset tonic response, never accompanied by a VWR. The VWR in SCI subjects was typically of much larger amplitude than the tonic responses and involved a mean of 5 muscles (41% bilaterally). Features of these responses provide an insight into underlying neurocontrol mechanisms which may provide guidance in the selection of appropriate intervention or management strategies.     

Quantitation of the stretch reflex

The stretch reflex should ideally be quantitated for better clinical use by standardizing the muscle stretch and measuring the resulting muscle contraction. Quantitation of muscle contraction can be done by force measurements or electromyographic recordings. The electromyographic response to stretch consists of one component (short latency response) for short stretches (less than 15 ms) and of 2 or 3 components (short and long latency responses) for longer stretches (greater than 40-50 ms). The magnitude of the phasic stretch reflex is reflected by the short latency response, whereas the magnitude of the tonic stretch reflex is reflected by both the short and the long latency responses. In clinical studies of upper motor neuron syndromes, the knee jerk and the muscle tone correlated with the magnitude of the short latency response. In patients with paralysis agitans an increased long latency response, which correlated to the rigidity, was found.     

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.     

THE MODE OF ACTION OF THE GABA DERIVATIVE BACLOFEN IN HUMAN SPASTICITY

Baclofen is chemically related to GABA and has proved to have a clinical effect on spasticity and on flexor spasms. The mode of action of baclofen was studied by quantitative measurements of some reflexes and of voluntary power in relation to intravenous injections of the drug (average dose 0.38 mg per kg body weight) in 44 patients with spasticity due to spinal or cerebral lesion or multiple sclerosis; a total of 53 injections were given. In most of the patients studied, depression occurred in the phasic stretch reflex (Achilles tendon), tonic stretch reflex, flexor reflex, reflexes from the pelvic floor and in the tonic vibration reflex; whereas the fl reflex changed in only a few cases, and voluntary power did not change at all. In some patients a pronounced increase was observed in the vibration-induced depression of the H reflex, which after baclofen approached normal. Baclofen can reduce the fusimotor drive, whereas a general primary effect on the α motoneurones is unlikely. It acts on the interneurones and can increase ‘presynaptic’ inhibition of the la nerve fibres. It is capable of exerting its action exclusively at the spinal level and can depress hyperactive stretch reflexes, whether they are caused by a spinal or cerebral lesion.     

Voluntary and reflex control of the biceps brachii muscle in spastic-athetotic patients

A cross-correlation technique of analysis was used to measure the transmission characteristics of tonic stretch reflex (TSR) pathways in spastic-athetoid subjects sustaining a voluntary contraction in the biceps brachii muscle. A comparison was made with the transmission characteristics of normal subjects measured by the same technique. It was found that gain and phase characteristics of spastic patients did not display the large resonant peaks present in normals. It is proposed that the resonant peaks in the TSR transmission of normal subjects were caused by long loop pathways. The absence of these peaks in the spastic patients supports the hypothesis that short-circuiting of long loop pathways by hyperactive spinal reflexes is part of the mechanism of spasticity.     

The pathophysiology of spasticity

Spasticity is only one of several components of the upper motor neurone (UMN) syndrome, known collectively as the `positive' phenomena, that are characterized by muscle overactivity. Other components include tendon hyper-reflexia, clonus, the clasp-knife phenomenon, flexor and extensor spasms, a Babinski sign, and spastic dystonia. Spasticity is a form of hypertonia due to hyperexcitable tonic stretch reflexes. It is distinguished from rigidity by its dependence upon the speed of the muscle stretch and by the presence of other positive UMN signs. Hyperactive spinal reflexes mediate most of these positive phenomena, while others are due to disordered control of voluntary movement or abnormal efferent drive. An UMN lesion disturbs the balance of supraspinal inhibitory and excitatory inputs, producing a state of net disinhibition of the spinal reflexes. These include proprioceptive (stretch) and nociceptive (flexor withdrawal and extensor) reflexes. The clinical syndrome resulting from an UMN lesion depends more upon its location and extent, and the time since it occurred, than on the pathology of the lesion. However, the change in spinal reflex excitability cannot simply be due to an imbalance in supraspinal control. The delayed onset after the lesion and the frequent reduction in reflex excitability over time, suggests plasticity in the central nervous system. Knowledge of the electrophysiology and neurochemistry of spinal reflexes, together with the action of antispasticity drugs, helps us to understand the pathophysiology of spasticity.