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Clinical assessment of spasticity in spinal cord injury: a multidimensional problem.

OBJECTIVE: To determine the relation between various components of spasticity evaluated clinically in persons with spinal cord injury (SCI). DESIGN: Case series evaluating spasticity using clinical scales commonly referenced in contemporary literature, including the Penn Spasm Frequency Scale, the Ashworth Scale, and standard scales of tendon taps, clonus, and plantar stimulation. SETTING. A Veterans Affairs Medical Center Spinal Cord Injury Center. PATIENTS. Eighty-five spinal cord injured individuals with varying degrees of spasticity. RESULTS: Correlations demonstrated weak relationships between Spasm Frequency Scale and self-report scales of interference with function (.407) and painful spasms (.312). No clinical examination score correlated with self-report scores greater than 0.4. Three clinical examination scores correlated modestly (> 0.5)-Ashworth score with patellar tendon taps (.553), ankle clonus with Achilles tendon tap (.663), and patellar tendon tap with adductor tendon tap (.512). Two other clinical scales correlated weakly (> 0.4)-Achilles tendon tap with patellar tendon tap (.417) and plantar reflex with adductor tendon taps (.423). CONCLUSIONS: Clinical scales currently used to evaluate spasticity in SCI correlate poorly with each other, suggesting that they each assess different aspects of spasticity. The use of any single scale is likely to underrepresent the magnitude and severity of spasticity in the SCI population. In the absence of agreement among these various scales and with the absence of an appropriate criterion standard for evaluation of spasticity, assessments of spasticity, whether clinical or neurophysiological in nature, should be comprehensive in scope.

Activities of Daily Living↗

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

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.(ABSTRACT TRUNCATED AT 250 WORDS)

Adult↗

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.

Adult↗

The effect of muscle paralysis on the radial growth of collagen fibrils in developing tendon.

Voluntary muscle activity in chick embryos was paralysed by administration in ovo of tubocurarine hydrochloride, administered in single or multiple doses, from day 9 to day 13 after fertilization. Control eggs were given saline instead of tubocurarine or were simply incubated without operative interference. Embryos were killed at 9, 13, 14, 16 and 19 days after fertilization. Flexor digitorum tendons were removed, fixed in glutaraldehyde, embedded in plastic, sectioned, and stained with phosphotungstic acid for electron microscopy. The diameters of the tendon collagen fibrils were measured, on electron micrographs, using a Magiscan Mk II programme. Tendon collagen fibril expansion was not inhibited by tubocurarine treatment. It is concluded that the rapid increase of collagen fibril diameters, which coincides in the normal embryo with the first onset of use of the associated muscle, is not dependent on muscle activity. There remains a possibility that other ways of producing tension in the tendon could provide sufficient stimulus to fibril expansion.

Animals↗

Spinal motoneuron excitability after acute spinal cord injury in humans.

BACKGROUND: Few studies in humans have assessed the ability of Ia afferent and antidromic motor volleys to activate motoneurons during spinal shock. Hence, little is known about the excitability state of the spinal motoneuron pool after acute spinal cord injury (SCI) in humans. METHODS: In 14 patients with acute SCI involving anatomic levels T10 and above, we performed clinical and electrophysiologic studies early after injury (within 24 hours in seven subjects) and on day 10, 20, and 30 postinjury. Maximal H:M ratios, F-wave persistence, and tendon tap T-reflexes were recorded. Sixteen normal subjects and eight chronic SCI patients served as control subjects. RESULTS: Ten of 14 patients had spinal shock (complete paralysis, loss of sensation, absent reflexes, and muscle hypotonia below the injury) at the time of initial evaluation. F-waves were absent in patients with spinal shock, reduced in persistence in patients with acute SCI without spinal shock, and normal in persistence in patients with chronic SCI. H-reflexes were absent or markedly suppressed in patients with spinal shock within 24 hours of injury but recovered to normal amplitudes within several days postinjury. This recovery occurred despite absence of F-waves that persisted for several weeks postinjury. Deep tendon reflexes were proportionally more depressed in spinal shock than were H-reflexes. All patients had elicitable H-reflexes for days or weeks before the development of clinical reflexes. CONCLUSIONS: Rostral cord injury causes postsynaptic changes (hyperpolarization) in caudal motoneurons. This hyperpolarization is a major physiologic derangement in spinal shock. The rise in H-reflex amplitude despite evidence of persistent hyperpolarization is due to enhanced transmission at Ia fiber-motoneuron connections below the SCI. Finally, the observation that the stretch reflex is proportionally more depressed than the H-reflex is consistent with fusimotor drive also being depressed after SCI.

Acute Disease↗

Interaction of excitatory and inhibitory inputs to motoneurons in man.

Two separate paradigms were used to study the interaction of excitatory and inhibitory inputs to the motoneuron pools of lower leg muscles in human subjects. During inhibition of tibialis anterior muscle from Ia soleus afferents, the probability of firing of the higher threshold unit decreased more than that of the lower theshold unit in 14 out of 18 pairs. When soleus motor units were recruited by tendon vibration reflex and the subject voluntarily inhibited one unit, the higher threshold unit was silenced first in 55 pairs, whereas the lower threshold unit ceased firing first in 29 pairs, and 16 showed inconsistencies. It is concluded that although under standard conditions there is orderly derecruitment of units which is the reverse of recruitment, vibration of the intact human tendon brings about synaptic effects in the spinal cord which affect the normal patterns of recruitment and derecruitment of motor units.

Adult↗

Persisting changes in sensory and motor activity of a muscle following its reflex activation.

A study was made to see if contractions induced by reflex action were followed by an elevation in muscle afferent activity comparable to the post-contraction sensory discharge (PCSD) that occurs after stimulation of the ventral roots. In lightly anesthetized cats, extension reflexes of the triceps surae muscle in the otherwise denervated leg were induced by contralateral stimulation of the popliteal nerve or footpad. The reflex response was followed by an elevated afferent discharge, which disappeared after a brief stretch, as is characteristic also of the PCSD. Crossed-extension responses in fusimotor activity unaccompanied by contraction of the gross muscle were also succeeded by an elevation in sensory discharge and an increased sensitivity to a vibratory stimulus applied to the tendon. Pinna reflexes had a similar effect. In the presence of the elevated discharge, alpha-motoneurons demonstrated increased sensitivity to vibration stimuli. It is suggested that the increase in spindle sensitivity may help stabilize the muscle against minor pertubations in length, at least when background fusimotor activity is relatively quiet.

Animals↗

A large-scale model of some spinal reflex circuits.

This paper reports the development of a large-scale model of some spinal reflex circuitry, useful for studying the dynamic interactions among neuronal populations during simple behaviors. The included populations and properties of the neurons and terminals were derived from the literature, mainly on cat spinal cord. The model was conceived as a symmetrical controller of a pair of antagonistic muscles, within the behavioral domain of the stretch and Golgi-tendon-organ reflexes, and was scaled to include realistic numbers of motoneurons. Inputs to the model were fiber populations providing random synaptic drive to some of the populations and sensory stimuli appropriate for the reflexes. The resulting model contained roughly 2300 neurons in six pairs of populations. The total number of connections in the model was about 600,000, and individual postsynaptic potentials were small (0.1-0.6 mV). Model responses were calibrated by examination of their ability to reproduce known aspects of the reflexes. Published algorithms were used to construct the environment, which is easily expandable, in terms of membrane channels, neuronal geometry, and synaptic properties. The system was built to combine a system-level perspective of spinal circuitry with the single-unit perspective common in electrophysiological investigation. It provides a computational tool for system-level investigations of spinal cord similar to the tools available at the level of membrane currents.

Animals↗

Chemical ablation of sensory afferents in the walking system of the cat abolishes the capacity for functional recovery after peripheral nerve lesions.

Weakening the ankle extensor muscles of cats by denervation of the synergists of the medial gastrocnemius (MG) muscle results in transient increase in yield at the ankle during early stance. Recovery of ankle function occurs over a period of 1-2 weeks, is use-dependent, and is associated with increases in the strength of reflexes from MG group I muscle afferents and an increase in the magnitude of bursts in the MG muscles during stance. These observations have led to the hypothesis that feedback from large muscle afferents is necessary for functional recovery. In this investigation we have tested this hypothesis by examining functional recovery in animals treated with pyridoxine, a drug known to destroy large muscle afferents. In four adult animals we confirmed that pyridoxine abolished the group I-mediated tendon-tap reflex in the ankle extensor muscle, and subsequently found that group I afferents from MG were either destroyed or non-conducting. Immediately after pyridoxine treatment the animals showed severe locomotor dysfunction but all recovered significantly over a period of 1 or 2 months and showed only minor kinematics deficits at the time of the muscle denervations. In all four pyridoxine-treated animals, weakening of the ankle extensors by denervation of the synergists of the MG muscle resulted in a large increase in yield at the ankle that persisted almost unchanged for a month after the operation. The magnitude of burst activity in the MG muscle during early stance of the pyridoxine-treated animals either did not increase or increased only slightly after the denervation of synergists. These observations are consistent with the hypothesis that feedback from group I afferents is necessary for functional recovery in untreated animals.

Afferent Pathways↗

Coding of pulsatile motor output by human muscle afferents during slow finger movements.

1. Impulse activities of thirty-eight muscle spindle and tendon organ afferents from the finger extensor muscles were recorded in the radial nerve of human subjects while the subjects performed voluntary flexion and extension finger movements at a single metacarpophalangeal joint. 2. The afferent firing was analysed in relation to the 8-10 Hz discontinuities which previously have been shown to characterize these movements. Spike-triggered averaging and frequency domain analyses demonstrated that all Ia muscle spindle afferents and a large proportion of group II spindle afferents responded in close association with local peaks in the joint acceleration. During muscle lengthening the impulses appeared during phases of rapid muscle stretch, whereas they appeared during the phase of minimal speed during muscle shortening. 3. The Golgi tendon organ (Ib) afferents displayed a reverse pattern of activity in relation to the discontinuities, i.e. the impulses tended to appear in the phase of minimal speed during lengthening movements and close to maximal shortening speed during shortening movements. Hence, their firing often coincided with the phasic increases of the parent muscle activity which account for the 8-10 Hz discontinuities. 4. A close analysis of the time relations between spindle firing and the kinematics of the 8-10 Hz discontinuities revealed that the population spindle response was too delayed and too dispersed to support the hypothesis that the discontinuities are accounted for by the stretch reflex. 5. If, as suggested in a previous paper, the 8-10 Hz discontinuities are produced by a pulsatile descending motor command, the coding of the periodic but tenuous kinematic events by the population of proprioceptors may have a role in relation to an alleged pulsatile command generator.

Adult↗

Forearm muscles of man can reverse their function after tendon transfers: an electromyographic study.

In patients suffering from paralysis of a major synergistic muscle group tendon transfers can be considered the therapy of choice in restoring the mobility of the affected joint(s). In order to study the mechanisms underlying the subsequent reversal of function in the transferred muscles, we have recorded the EMG of several forearm muscles in parallel and compared their activation periods with control data from healthy volunteers. Slow and fast extension-flexion movements of the wrist were evaluated. The findings demonstrated a 'new' phasic EMG activity within the transferred muscles, which correlated to their new mechanical function. However, the 'old' EMG pattern was not lost. In some muscles it was present in fast and slow wrist movements, in others only in fast ones. The results indicate that the reversal of function observed in the transferred muscles can be adjusted to meet the specific needs of the movement to be performed.

Adaptation, Physiological↗

Scratch responses in normal cats: hindlimb kinematics and muscle synergies.

1. Scratch responses evoked by a tactile stimulus applied to the outer ear canal were characterized in nine adult cats. Chronic electromyographic (EMG) electrodes were surgically implanted in selected flexor and extensor muscles of the hip, knee, and ankle joints to determine patterns of muscle activity during scratching. In some trials EMG records were synchronized with kinematic data obtained by digitizing high-speed ciné film, and in one cat, medial gastrocnemius (MG) tendon forces were recorded along with EMG. For analysis the response was divided into three components: the approach, cyclic, and return periods. Usually scratch responses were initiated with the cat in a sitting position, but in some trials the animal initiated the response from a standing or lying posture. 2. During the approach period the hindlimb ipsilateral to the stimulated ear was lifted diagonally toward the head by a combination of hip and ankle flexion with knee extension. Hindlimb motions during the approach period were associated with sustained EMG activity in hip-flexor, knee-extensor (occasionally), and ankle-flexor muscles. Initial hindlimb motions were typically preceded by head movements toward the hindpaw, and at the end of the approach period, the head was tilted downward with the stimulated pinna lower than the contralateral ear. During the return period movements were basically the reverse of the approach period, with the hindpaw returning to the ground and the head moving away from the hindlimb. 3. During the cyclic period the number of cycles per response varied widely from 1 to 60 cycles with an average of 13 cycles, and cycle frequency ranged from 4 to 8 cycles/s, with a mean of 5.6 cycles/s. During each cycle the paw trajectory followed a fairly circular path, and the cycle was defined by three phases: precontact, contact, and postcontact. On average the contact phase occupied approximately 50% of the cycle and was characterized by extensor muscle activity and extension at the hip, knee, and ankle joints. The hindpaw contacted the pinna or neck at the base of the pinna throughout the contact phase, and paw contact typically resulted in a rostral motion of the head as the hindlimb extended. 4. The postcontact phase constituted approximately 24% of scratch cycle and was usually initiated by the onset of knee flexion. Ankle and then hip flexion followed knee flexion, and flexor muscles were active during the postcontact phase as the paw was withdrawn from the head. The precontact phase constituted approximately 26% of scratch cycle and was initiated by knee joint extension and knee-extensor activity.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Baclofen, a new antispastic drug. A controlled, multicenter trial in patients with multiple sclerosis.

A double-blind, five-week, multicenter trial was conducted to compare the effect of baclofen, a unique amino acid derivative, with that of placebo in the treatment of 106 patients with spasticity secondary to multiple sclerosis. A spasticity assessment method that included a neurological examination, physicians' clinical impressions of changes during treatment, and a patient's self-evaluation was used to determine efficacy. This method showed baclofen (70 to 80 mg daily maximum, titrated) is effective relative to placebo in relieving symptoms of spasticity, such as flexor spasms, pain and stiffness, resistance to passive joint movements, and tendon stretch reflexes. Patient self-evaluation results also showed a significant reduction in clonus. Side effects were generally mild and transient.

Adolescent↗

Characterization of hamstring reflexes during anterior cruciate ligament disruption: in vivo results from a goat model.

The existence of an anterior cruciate ligament-hamstring reflex arc, the extent to which these reflexes can protect the knee, and the extent to which they are affected by rupture of the anterior cruciate ligament remain controversial. We evaluated the temporal components of the anterior cruciate ligament-hamstring synergy by simulating an injury to the ligament in a goat model. Reflexive hamstring activation in anesthetized goats was evaluated when the anterior cruciate ligament was loaded with static subfailure, dynamic subfailure, and dynamic failure loads. Reflexive hamstring activation was not found in response to static subfailure loading but was observed in response to dynamic subfailure and failure loading. The latency of the reflex evoked by dynamic failure loading was shorter than that evoked by dynamic subfailure loading. The findings suggest that the extent to which the hamstring reflexes can protect the knee may be bounded by the ability of these muscles to generate force rapidly and the amplitude and time-course of the loads applied to the knee joint. The present data present a framework for further investigation of the contribution of anterior cruciate ligament-hamstring reflexes to the stability of the knee joint under high loads and loading rates.

Animals↗

Development of a human neuro-musculo-skeletal model for investigation of spinal cord injury.

This paper describes a neuro-musculo-skeletal model of the human lower body which has been developed with the aim of studying the effects of spinal cord injury on locomotor abilities. The model represents spinal neural control modules corresponding to central pattern generators, muscle spindle based reflex pathways, golgi tendon organ based pathways and cutaneous reflex pathways, which are coupled to the lower body musculo-skeletal dynamics. As compared to other neuro-musculo-skeletal models which aim to provide a description of the possible mechanisms involved in the production of locomotion, the goal of the model here is to understand the role of the known spinal pathways in locomotion. Thus, while other models focus primarily on functionality at the overall system level, the model here emphasizes functional and topological correspondance with the biological system at the level of the subcomponents representing spinal pathways. Such a model is more suitable for the detailed investigation of clinical questions related to spinal control of locomotion. The model is used here to perform preliminary experiments addressing the following issues: (1) the significance of spinal reflex modalities for walking and (2) the relative criticality of the various reflex modalities. The results of these experiments shed new light on the possible role of the reflex modalities in the regulation of stance and walking speed. The results also demonstrate the use of the model for the generation of hypothesis which could guide clinical experimentation. In the future, such a model may have applications in clinical diagnosis, as it can be used to identify the internal state of the system which provides the closest behavioral fit to a patient's pathological condition.

Computer Simulation↗

Flexion reflexes following anterolateral cordotomy in man: dissociation between pain sensation and nociceptive reflex RIII.

Nociceptive flexion reflexes (RIII response) of the lower limbs were recorded after unilateral cervico-thoracic anterolateral cordotomy (ALC) in 7 patients. Pre-operative recordings were also obtained in 1 patient and follow-up observations in 3 patients. Flexion reflexes ipsilateral to cordotomy remained normal after surgery. Conversely, responses contralateral to the cordotomy exhibited two consistent postoperative changes: first, the RIII reflex was always dissociated from subjective pain, i.e., it appeared in the absence of any pain sensation, and, second, the RIII was depressed in the limb contralateral to ALC in 5 of 7 patients. RIII attenuation ranged from slight reduction to total abolition, and proved to be reversible in 2 of 3 patients tested during the follow-up. The reappearance of withdrawal reflexes was never accompanied by a recovery of pain sensation in the stimulated limb. We conclude that the dissociation between flexion reflexes and pain sensation, which was evidenced even in case of depressed RIII responses, should be attributable to the surgical lesion of spinothalamic fibers. Dissociation between RIII and subjective pain is a landmark indicating a lesion of the spinothalamic fibers, and may be used for the clinical assessment of spinothalamic dysfunction. Conversely, RIII depression after ALC does not depend upon the surgical lesion to the spinothalamic axons, but may be secondary to interruption of ascending spinoreticular fibers in the anterolateral quadrant, and/or of descending excitatory axons in the ventral cord.

Adult↗