Abstract: Spasticity is a disorder of the sensorimotor system characterized by a velocity-dependent increase in muscle tone with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex. It is one component of the upper motoneuron syndrome, along with released flexor reflexes, weakness, and loss of dexterity. Spasticity is an important “positive” diagnostic sign of the upper motoneuron syndrome, and when it restricts motion, disability may result. The “negative” signs—weakness and loss of dexterity—invariably alter patient function when they occur. In an upper motoneuron syndrome, the alpha motoneuron pool becomes hyperexcitable at the segmental level. This hyperexcitability is hypothesized to occur through a variety of mechanisms, not all of which have yet been demonstrated in humans. Spasticity caused by spinal cord lesions is often marked by a slow increase in excitation and overactivity of both flexors and extensors with reactions possibly occurring many segments away from the stimulus. Cerebral lesions often cause rapid build-up of excitation with a bias toward involvement of antigravity muscles. Chronic spasticity can lead to changes in the rheologic properties of the involved and neighboring muscles. Stiffness, contracture, atrophy, and fibrosis may interact with pathologic regulatory mechanisms to prevent normal control of limb position and movement. In the clinical exam, it is important to distinguish between the resistance due to spasticity and that due to rheologic changes, because the distinction has therapeutic implications. Diagnostic nerve or motor point blocks and dynamic or multichannel EMG are useful to distinguish the contributions of spasticity and stiffness to the clinical problem. ©1997 John Wiley & Sons, Inc. Spasticity:Etiology, Evaluation, Management, and the Role of Botulinum Toxin Type A, MF Brin, editor. Muscle Nerve 1997; 20 (suppl 6):S1-S13. Keywords: spasticity, upper motoneuron syndrome (UMN syndrome), spasticity pathophysiology, stretch reflex, rheologic properties of muscle, diagnostic nerve blocks, dynamic EMG
Clinicophysiologic Concepts of Spasticity and Motor Dysfunction in Adults with an Upper Motoneuron Lesion Nathaniel H. Mayer, MD
Spasticity and the Stretch Reflex A century ago, Sherrington transected a cat’s brain stem above the vestibular nuclei to produce an animal with increased stretch reflexes and tone in the antigravity extensor muscles.21,22 Despite complete brain stem transection, the cat retained the ability to stand on all fours with rigid legs. Based on the above features, it was said to have “decerebrate rigidity.” Since then, rigidity has been shown to be influenced by afferent impulses as well as by descending signals within the central nervous system. Sherrington himself was able to eliminate rigidity in a limb by cutting its dorsal roots. Although animal “decerebrate rigidity” is not considered analogous to human adult spastic states, Sherrington’s seminal studies of the cat’s myotatic stretch reflex established the model of an afferent-efferent neural circuit as the basis for understanding changes in stretch reflex activity. Sherrington’s model provided strong physiologic underpinnings for later clinical descriptions of spastic signs and symptoms. Peter Nathan’s description of spasticity emphasizes the central role of the stretch reflex as follows: “Spasticity is a conNathaniel H. Mayer, MD Drucker Brain Injury Center MossRehab Hospital 1200 West Tabor Road Philadelphia, PA 19141-3019
dition in which stretch reflexes that are normally latent become obvious. The tendon reflexes have a lowered threshold to tap, the response of the tapped muscle is increased, and usually muscles besides the tapped one respond; tonic stretch reflexes are affected in the same way.”16 Nathan’s description refers to an increase in phasic stretch reflexes (tendon jerks) and tonic stretch reflexes (resistance to passive stretch appreciated by the examiner as muscle tone). The key point is the exaggerated or “positive” nature of the motor response that is elicited by the clinician during examination. For historical reasons, and because hyperreflexia and hypertonias are so useful in pointing to the presence of an upper motoneuron lesion, stretch reflexes are a common starting point for discussions of spasticity, even while recognizing that other associated phenomena often have more impact on patient functioning. An increased stretch reflex may occur because the alpha motoneuron pool at the segmental level is hyperexcitable; or the amount of excitatory afferent input elicited by muscle stretch is increased; or both. The motoneuron pool is considered hyperexcitable if less than standard excitatory input suffices either to bring motoneurons to the firing threshold or to increase their firing frequency. This hyperexcitability may be generated by a change in the balance of excitatory and inhibitory inputs to the motoneuron pool. In an upper motoneuron lesion, it is theorized that inhibitory inputs
KEY POINTS • Alpha motoneuron hyperexcitability may be caused by reduced inhibitory input, denervation supersensitivity, shortening of motoneuron dendrites, or collateral sprouting of dorsal root afferents
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are reduced, thereby generating hyperexcitability. Shortening of motoneuron dendrites and collateral sprouting of dorsal root afferents may also play a role in alpha motoneuron pool hyperexcitability.1,10,17 Though gamma motor system theories have long been popular, there seems to be no direct evidence supporting the idea that increased fusimotor drive on spindle afferents occurs to enhance the stretch reflex.1
in patients with an upper motoneuron lesion. Moreover, these predominantly sensory driven motor phenomena can be problematic to patients and are legitimate objects of treatment. For example, bladder stones in the urinary tract of a paraplegic patient can trigger severe and unwanted flexor spasms that interfere with activities of daily living. Yawning in a hemiplegic patient (who ordinarily has persistent elbow, wrist, and finger flexion) can trigger unexpected elbow, wrist, and finger extension. I once had a patient who broke a finger against a doorway arch in just such a forceful extensor episode!
This afferent-efferent neural model of the stretch reflex has served clinicians well by allowing them to infer the presence of an upper motoneuron lesion when spasticity is present. In fact, spasticity is most commonly The Upper Motoneuron understood and appreciated in terms of its Syndrome: Positive and Negative diagnostic implications. After members of a Symptoms symposium on the topic reached consensus, Lance published this frequently-cited defini- Spasticity as a clinical sign needs to be distion: “Spasticity is a motor disorder charactinguished from spasticity as one factor terized by a velocity-dependent increase in among others that contribute to motor dystonic stretch reflexes (muscle tone) with function in the presence of an upper exaggerated tendon jerks, resulting from motoneuron lesion. Kuypers has demonhyperexcitability of the stretch reflex, as one strated in the monkey that isolated lesions component of the upper motoneuron synof the pyramidal tract above the foramen drome.”13 It is clear that the defining charac- magnum do not increase muscle tone but teristic of clinical spasticity is the examiner’s they do cause a loss of dexterity, particularly perception that passive stretch of a muscle in distal musculature, and they severely group generates excessive resistance, which impair finger fractionation (discrete finger goes up as the examiner increases the rate of movements).12 In humans, it is generally stretch. But note that Lance also identifies believed that an upper motoneuron lesion the larger diagnostic context in which spas- not only damages the pyramidal tract, but tic reflexes are typically found, namely, the also other nearby motor pathways such as upper motoneuron (UMN) syndrome. As a the cortico-reticulospinal tract. Damage to term, though, “spasticity” often keeps even these tracts gives rise to increased alpha broader company. In a general way, it is motoneuron excitability at the segmental clear from the work of Sherrington and cord level with a resulting increase in musmany others that the exaggerated motor cle tone and tendon jerk responses. response of the spastic patient originates from changes in the way in which segmental According to Lance, the four distinguishing spinal cord circuitry handles information features of the upper motoneuron syndrome from a variety of sources, including proprio- are the positive symptoms of 1) enhanced ceptive, exteroceptive, and suprasegmental stretch reflexes (spasticity) and 2) released descending input.23 “Spasticity” may have a flexor reflexes in the lower limbs; and the particular affiliation with the stretch reflex negative symptoms of 3) loss of dexterity arc, but every clinician is familiar with and 4) weakness (see Table 1).14 adventitial reflex movements, not strictly myotatic in origin, that occur at the bedside
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KEY POINTS • As one component of the upper motoneuron syndrome, spasticity is a motor disorder characterized by a velocitydependent increase in tonic stretch reflexes (muscle tone) with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex • Disorders which may lead to an upper motoneuron syndrome: cerebral palsy, multiple sclerosis, traumatic brain injury, stroke, spinal cord injury, neurodegenerative diseases
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KEY POINTS
Figure 1.
• The UMN syndrome includes the positive symptoms of spasticity and released flexor reflexes, and the negative symptoms of loss of dexterity and weakness • The negative symptoms are often more important to the function of the patient than the positive ones
1) Enhanced Stretch Reflexes Enhanced stretch reflex activity may be manifested by increased muscle tone (tonic or sustained stretch reflex activity), exaggerated tendon jerks (phasic stretch reflexes), spread or irradiation of phasic stretch reflexes in response to tendon hammer percussion, and repetitive stretch reflex discharges or clonus generated by sustained stretch. Many of these phenomena can be understood in the context of muscle spindle physiology (see Figure 1). Primary afferent Ia fibers surrounding intrafusal fibers of the muscle spindle are excited when a muscle is stretched. The Ia fiber makes a monosynap-
tic excitatory connection with alpha motoneurons of its muscle of origin, and it similarly connects with alpha motoneurons of synergistic muscles. The Ia fiber also monosynaptically connects with an inhibitory interneuron that projects directly to the alpha motoneurons of antagonist muscles. When a muscle is stretched, excitation of homonymous and synergistic motoneurons, combined with inhibition of antagonists, subserves the mechanism of reciprocal inhibition. There is evidence for impairment of this mechanism in the UMN syndrome.2 The literature discusses two clinical forms
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Table 1.
Clinical Features of Movement Dysfunction in the Upper Motoneuron Syndrome POSITIVE SYMPTOMS Spasticity increased muscle tone exaggerated tendon jerks stretch reflex spread to extensors repetitive stretch reflex discharges; clonus
Released flexor reflexes Babinski response mass synergy patterns
NEGATIVE SYMPTOMS Loss of finger dexterity Weakness inadequate force generation slow movements
Loss of selective control of muscles and limb segments
RHEOLOGIC CHANGES IN SPASTIC MUSCLE Stiffness Contracture Fibrosis Atrophy of spasticity, a spinal model and a cerebral model, whose underlying physiological differences stem from differences in how peripheral afferent activity is handled centrally. Spinal Model: Using repetitive sinusoidal stretching of calf muscles, Herman et al. found that patients with spinal cord lesions had a relatively slow rise of reflex activity compared to cerebral model patients, with peak activity occurring only after a number of stretch cycles were generated.7 He attributed this relatively slow rise to a slow, progressive increase in the excitatory state of the spinal cord by cumulative, stretch-generated excitation in interneuronal pathways. He argued that cord lesions removed inhibitory influences on segmental polysynaptic pathways with the likely result that primary afferent discharges from the muscle spindle were transmitted through multisynaptic chains of the interneuronal pool.
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In the spinal model, afferent activity, be it from muscle spindles or from flexor reflex afferents (see below), enters the cord at one level but then ascends or descends without inhibition to other levels of the cord, resulting in muscle responses many limb segments removed from the afferent generators originally stimulated. For example, it is not unusual for S1 nociceptive stimulation of the foot of a paraplegic to generate L5 knee flexor, L2 hip flexor, and T10 abdominal muscle contraction. Even though strong flexor muscles tend to dominate clinical movement patterns, cumulative excitation in the cord may spill over to flexor and extensor muscle groups.
KEY POINTS • Spasticity, spinal model: —removal of inhibition on segmental polysynaptic pathways —slow, progressive rise of excitatory state through cumulative excitation —afferent activity from one segment may lead to muscle response many segments away —flexors and extensors may be overexcited
Cerebral Model: In contrast, Herman notes that in the cerebral (or hemiplegic) model of spasticity, sinusoidal stretching of calf muscles results in a rapid build-up of reflex activity, suggesting that transmission of primary ending spindle discharges occurs
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largely through monosynaptic pathways. Clinically, cerebral model patients often demonstrate recognizable antigravity postural patterns characterized by shoulder adduction and elbow and wrist flexion in the upper limb, and by hip adduction, knee extension and ankle plantar flexion, reflecting extension posture in the lower limb.15 This “hemiplegic” posture is thought to result from increased motoneuron activity in antigravity muscles (i.e., flexors in the upper limb and extensors in the lower limb when the patient stands upright “against gravity”). Antigravity muscles are typically spastic to passive examination, but it is not entirely clear whether their postural attitude reflects mishandling of peripheral afferent drive in spinal circuits or results from inappropriate descending signals. Sectioning dorsal roots does not necessarily abolish the posture or its associated activity in antigravity muscles.4 2) Released Flexor Reflexes According to Lance, the flexor reflex is a polysynaptic reflex mediated by myelinated group II fibers originating from the muscle spindle and by unmyelinated group IV afferent fibers. Group IV afferents generally carry information from touch and pressure receptors in skin, joint receptors, nociceptors, and muscle spindles. Collectively referred to as flexor reflex afferents, they activate a reflex pathway that excites flexor motoneurons and inhibits extensor motoneurons. The flexor reflex is inhibited by the dorsal reticulospinal tract and facilitated by corticospinal and rubrospinal pathways.20
a related flexor release phenomenon, is a clinical problem that reflects persistent activity in extensor hallucis longus and is usually amenable to treatment by chemodenervation. Flexor reflex afferents have numerous polysynaptic connections that spread intersegmentally through the spinal cord, and so a localized stimulus in the foot or leg can generate widespread flexor and adductor spasms. Widespread muscle involvement usually requires a regional or systemic treatment strategy. As a result, systemic or intrathecal drugs have often been preferred. However, selective muscle interventions with neurolytic or chemodenervation agents, aimed at adductors, hamstrings or other critically involved muscle groups may be sufficient to blunt the patient’s clinical problem. 3&4) Loss of Finger Dexterity and Weakness Loss of finger dexterity and weakness are the two most important negative symptoms brought on by an upper motoneuron lesion.1 The ability to make selected or isolated movements across specific joints is usually severely impaired. Patients more often perform stereotypic whole limb movements characterized by obligatory linkages referred to as mass flexor and extensor “synergy” patterns. These obligatory limb synergies vary in their degree of stereotypy and, with recovery, evolve toward greater selective control over the degrees of freedom available at individual joints.
In the UMN syndrome, it is commonly observed that movement is slow, even after movement differentiation has recovered conClinically, the flexor reflex synergy includes siderably. Work at the motor unit level has big toe extension, and ankle, knee, and hip shed some light on the pathophysiology of flexion. Abdominal muscle contraction may weakness and slowness. Hoefer and Putnam also be seen. The Babinski response is seen showed as early as 1940 that in spastic muswhen flexor reflexes are released from brain cles, the number of motor units recruited in stem or cortico-reticulospinal inhibition. In a voluntary contraction is reduced, as is the its most diminutive form (great toe extenfiring frequency of these motor units.8 sion and toe fanning alone), it has been con- Moreover, once a motor unit is recruited, its sidered a fractional manifestation of the larg- discharge rate is often difficult to sustain. er flexor reflex. Hitchhiker’s toe (see below), Inadequate recruitment of motor units may
KEY POINT S • Spasticity, cerebral model: —enhanced excitability of monosynaptic pathways —rapid build-up of reflex activity —bias toward overactivity in the antigravity muscles and the development of hemiplegic posture •The clinical features of released flexor reflex are: —big toe extension (principal component of Babinski's sign) —ankle, knee, and hip flexion —contraction of abdominals
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result in an inability to generate sufficient force for functional purposes. In addition, a loss of orderly recruitment and rate modulation of motoneurons within a given motoneuron pool may lead to inefficient muscle activation.10 Paresis, therefore, reflects fundamental alterations in the functional control properties of the voluntary motor system. Many clinicians feel that defective function in the UMN syndrome is attributable more to the negative symptoms affecting the production and control of voluntary goal-directed movement than to the positive features that may include abnormalities of posture, spasticity, and exaggerated exteroceptive reflexes.1,19 The balance of positive and negative symptoms in a particular patient should influence selection of the appropriate treatment.
Movement Dysfunction in the Upper Motor Neuron Syndrome In patients with a UMN lesion, the clinical problems of movement dysfunction arise from a complex interaction among positive symptoms, negative symptoms, and changes in the physical properties of muscle and other tissues chronically subjected to positive and negative behaviors. Spasticity, impaired mechanisms of movement production, muscle stiffness, and contracture all contribute to a net imbalance of forces affecting joint position statically and limb movement dynamically. Stiffness and contracture involve the properties of plasticity and visco-elasticity, collectively termed “rheologic” properties. Changes in the rheologic properties of muscle, tendons, and joints can be caused by pathologic states that alter the normal control of limb position and movement. These rheologic changes can, in turn, exacerbate these pathologies. Nonreflex properties of muscle produce a resistance that increases with muscle length
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and with the velocity of stretch.18 In humans, Herman has shown that contractured spastic muscle, though declining in reflex activity, has an enhanced viscous reaction that contributes to the “tone” experienced by the examiner of such a patient.6 Herman viewed these changes as arising from changes in muscle itself. In studies of chronic human spasticity, Hufschmidt and Mauritz9 attributed series elastic forces within muscle to cross-bridge links between actin and myosin filaments, while other elastic forces were attributed to connective tissue elements. Plastic resistance was thought to result from histologic transformations such as fibrosis, atrophy, and changes in the contractile properties of certain muscle fiber types. In animal models, fixation of a muscle in a shortened state causes reversible loss of sarcomeres and increased stiffness.5 The clinical implication of such studies is that while spastic tension in a patient with recent onset of spasticity (before contracture and stiffness have set in) reflects primarily reflex-induced resistance, chronically spastic muscle often features both reflex resistance and resistance of rheologic origin. Muscle tone or resistance to stretch as experienced by the clinical examiner depends not only on the “active” contractile tension generated by reflex activity but on the “passive” tension generated by the rheologic properties of muscle and other tissues also being stretched. Clinical examination usually provides good information on reflex reactiveness, and clinical perceptions of tone and examining range of motion usually enable clinicians to make solid inferences regarding the presence of contracture. When the patient makes active movements, however, it may be more difficult by observation alone to distinguish among contributions of agonist muscle paresis, tension generated by spastic antagonists, and stiffness of antagonists due to rheologic changes.
KEY POINTS •Selective control of muscle groups may be replaced by mass synergies (obligatory patterns of movement) • Loss of finger and thumb dexterity often endures even after good proximal recovery in the upper limb • The rheologic properties of muscle— plasticity and visco-elasticity— also influence the control of muscle • Rheologic changes include stiffness, contracture, atrophy, and fibrosis
A number of strategies are useful for teasing
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Figure 2.
Repetitive finger flexion and extension performed by a 21-year-old man who sustained traumatic brain injury one year earlier.
FDS=flexor digitorum sublimis; FDP= flexor digitorum profundus; EDC=extensor digitorum communis
apart these contributions. Nerve blocks which eliminate reflex tension may help the clinician assess the remaining contribution of passive rheologic resistance from antagonist muscles. Kinesiologic electromyographic studies may help identify dynamic activity in antagonist muscles during movement, as well as demonstrate abnormalities in EMG recruitment associated with paresis. Using surface or wire electrodes, a one, two, or multichannel electromyographic amplifier system is useful in recording agonist and antagonist contributions to movement dysfunction. Such recordings help formulate a working question about the nature of restricted movement in any given case: namely, is motion limited because of weak agonists, or restrained by dyssynergic (“out of phase�) or spastic antagonists? For example, in Figure 2, repetitive cycles of active finger flexion and extension are displayed for a 21-year-old man who sustained traumatic brain injury (TBI) 1 year earlier. The record shows that activity in flexor digitorum sublimis (FDS) is appropriately in
phase while activity in flexor digitorum profundus (FDP) reflects poor recruitment during flexion phase and a lack of reciprocal inhibition during extension phase. Clinically, the finger flexors were tight and created the suspicion that, in addition to reflex activity, increased stiffness may be playing a role in limiting finger extension. The active range of motion was small, especially when the wrist was held in neutral position. Figure 3 shows wire electrode recordings obtained from a 38-year-old woman who sustained severe TBI 17 years earlier. She had a flexed wrist deformity along with an intrinsic plus resting posture (metacarpophalangeal [MCP] joint flexion, proximal interphalangeal [PIP] joint extension). Although she does not extend her MCP joints, she can nevertheless flex and extend her PIP and distal interphalangeal (DIP) joints. The figure reveals excellent EMG recruitment in extensor digitorum communis (EDC), and good extension motion across the PIP joint, but there is electromyographic coactivation of FDS. The behavior of
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Figure 3.
KEY POINTS
Active finger extension performed by a 38-year-old woman who had sustained traumatic brain injury 17 years earlier. Note coactivation of FDS during extension.
FDS=flexor digitorum sublimis; FDP= flexor digitorum profundus; EDC=extensor digitorum communis
FDP during finger extension is clearly less problematic than FDS, illustrating that spastic activity may vary in different muscles crossing the same joints. Different muscles and perhaps even different parts of the same muscle may contribute differentially to the net balance of forces that defines the clinical problem.
Clinical Applications Weakness of agonists and out-of-phase activation of antagonists are basic issues the clinician must consider in the UMN syndrome when evaluating a patient’s potential for movement. Both types of problems may diminish the net force across a joint and impair motion, thereby impairing active movement. Coactivation of antagonist muscles after upper motoneuron dysfunction is a well-recognized clinical and neurophysiological finding.11 In the clenched fist deformity, for example, it is common to find that FDS is activated when patients attempt to extend their fingers (see Figure 3). The finger extensors, variably paretic but usually not completely paralyzed, may fail to extend the fingers not because of paresis but because simultaneous activation of FDS antagonizes the extension effort. In the
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UMN syndrome, impaired reciprocal inhibition at the segmental level (as explained above) is one explanation offered for the presence of antagonist activity and the resulting movement dysfunction. Passive stretch of a spastic muscle by the examiner reveals that the stretch reflex has a lowered threshold. Passive stretch of a spastic muscle by the patient during the course of an active agonist-generated movement reveals a dysregulation of stretch reflex activity in antagonist muscles. The clinical effect of antagonist contraction is to offset and mask agonist-induced motion during voluntary effort. After an upper motoneuron lesion, individual muscles may be spastic (stretch-reactive) and volitional; i.e., the patient may be able to activate individual muscles through selfgenerated effort. As indicated above, poor motor unit recruitment is clinically associated with weakness of force generation, and a muscle that is poorly activated will have a negative impact on the multi-joint movement synergies with which that muscle is ordinarily associated (see Figure 2).
• Rheologic changes and pathologic regulatory mechanisms interact to prevent normal control of limb position and movement • Resistance in recent-onset spasticity is reflex-induced, while resistance in chronically spastic muscle involves rheologic changes such as increased stiffness • The sources of resistance encountered in active movements can be difficult to interpret
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In a circumstance of isolated muscle weakness, the nervous system may be able to compensate for such weakness by recruiting and organizing other muscle groups to achieve similar results, usually through alternative, compensatory movement patterns. The inability to extend the elbow in order to place the hand on a table top, for example, may result in compensatory hip flexion by the patient as he or she leans over the table top to place the hand at the desired location. Compensatory behaviors in lower motor neuron lesions (e.g., polio or peripheral neuropathy) are readily identified through clinical observation and manual muscle testing, and they often allow the patient to successfully achieve real motor objectives. In upper motoneuron lesions, however, separation of obligatory motor behavior from compensatory behavior is much trickier. Proximal and distal musculature are typically but variably involved by upper motoneuron pathology. Consequently, the nervous system’s ability to recruit and organize different muscle groups for compensatory purposes may be limited. Because of the UMN lesion, muscle groups ordinarily recruited for compensatory purposes may themselves be under only partial voluntary control as agonists, and they may be spastic as antagonists. Voluntary control in such situations is likely to be convoluted by an intermingling of compensatory and obligatory behaviors, producing problematic and ineffectual movements. Moreover, motion across virtually all joints of the upper and lower extremities may be accomplished by more than one muscle. For example, the elbow may be flexed by the biceps, the brachialis, or the brachioradialis. The PIP joint of the fingers may be extended by extensor digitorum communis, dorsal interosseous, or the lumbricales. In UMN lesions, paresis and spasticity of individual muscles can be very variable. When many muscles cross a joint, the positive volitional and negative spastic contributions of each muscle must be
assessed in order to arrive at a rational treatment plan.
KEY POINTS
To summarize, deciphering the negative sign of “weakness” in the UMN syndrome mechanistically is complicated because the central nervous system, a sophisticated control system even when damaged, attempts to achieve its movement objectives through compensatory strategies. These strategies may themselves be convoluted mixtures of obligatory and compensatory motor behaviors. Consider the gait pattern of a hemiplegic with co-contraction of quadriceps and hamstrings during the period of single limb support in stance phase. Is the co-contraction a compensatory phenomenon to control the knee, prevent buckling, and compensate for “weakness”? Or is it obligatory (pathological) activity occurring because of impaired reciprocal inhibition secondary to the UMN lesion? It is often difficult to interpret such clinical phenomena definitively when they occur by themselves. A clinician is better served by testing his or her interpretation as a working hypothesis. When findings suggest inappropriate EMG activity in an antagonist muscle during movement, diagnostic nerve or motor point block to the specific muscle may be performed to assess the effect of diminishing spasticity on the production of movement. In just this way, the longer-lasting effects of neurolytic and chemodenervating agents such as phenol and botulinum toxin are well suited for clinical trials that test the role of putatively spastic antagonists in specific movement disorders.
• Diagnostic nerve or motor point block and EMG are useful to distinguish the contributions of spasticity and stiffness to the clinical problem
Question: Is voluntary movement attempted by agonist muscles being restrained by spastic activity in antagonist muscles? Strategy: Weaken the antagonism by chemodenervation and observe whether the patient is able to generate or improve that voluntary movement during the months the block will remain in effect. The longer term trial may also help clarify the value of the
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physiologic intervention to patient performance, information not readily available from the brief diagnostic block. After voluntary and spastic behaviors of target muscles have been identified, an important remaining question is how to titrate a chemodenervating agent such that the volitional capacity of a muscle acting as an agonist is preserved, but its spastic resistance when acting as an unwanted antagonist is broken. Developing guidelines for this titration will be an important goal for future studies.
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KEY POINTS • When many muscles cross a joint, the behavior of each must be assessed when developing a treatment plan
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Case History A 20-year-old unemployed food service worker sustained a head injury 7 months earlier in a motor vehicle accident. He developed a spastic left hemiparesis and was ambulatory with a cane when we first saw him. He complained that his left elbow flexed severely against his chest, especially during gait, and sometimes his fist became jammed against the side of his throat. Passive resistance to stretch at the elbow was graded as Ashworth 3 and motion was restricted to -80 degrees from full extension. Biceps and brachioradialis were palpably contractile. Dynamic EMG studies revealed moderate activation of biceps, brachialis, and brachioradialis during flexion effort and high activity during passive stretch. Activity in the three heads of the triceps was low during efforts at elbow extension. The referring clinician had raised the question of serial casting to reduce the obvious clinical contracture. However, in cases of severe spasticity, it is not feasible to apply serial casts without blocking spasticity first. Therefore, prior to casting, we planned to perform a musculocutaneous nerve block with bupivacaine to relieve spasticity in both the biceps and the brachialis followed by a motor point block of brachioradialis. (Bupivacaine was chosen because its effect would last from the morning, when we saw the patient, until the early afternoon, when the patient’s physical therapist was able to do the first serial cast.) However, during initial positioning efforts, it became clear that we could not gain access to the musculocutaneous nerve adjacent to the axillary crease because of pectoralis major spasticity. Therefore, we first applied motor point blocks to pectoralis major. Fifteen minutes after the blocks, the shoulder could be passively abducted 60 degrees, allowing sufficient access to block the musculocutaneous nerve. After the block, biceps softened considerably to palpation, but range of motion at the elbow did not improve. Brachioradialis was still massively tense to stretch. We then performed a motor point block of brachioradialis, which improved the patient’s passive range to about -65 degrees from full extension. About 45 minutes after the last block was completed, Ashworth resistance to passive stretch of the elbow flexors was graded as 1, signifying a continued increase in resistance. Because biceps and brachioradialis were very soft to palpation and repeat dynamic EMG revealed only scattered electrical potentials, the dynamic component of tone was considered to be negligible. Nevertheless, the patient’s “resting” position for the elbow was noted to be 90 degrees from full extension—not -65 degrees which was measured as the maximum passive range. The persistence of a positive Ashworth score and the 90 degree “resting” flexion posture are consistent with the notion that elimination of the dynamic component of spasticity will not necessarily eliminate passive tensile contributions to muscle tone contributed by the rheologic properties of muscle. Serial casting may be helpful as a treatment in such situations because of the prolonged stretch delivered by the cast to tissues with increased rheologic stiffness and fixed contracture.
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Bibliography 1. Burke D: Spasticity as an adaptation to pyramidal tract injury. Adv Neurol 1988; 47:401-423. 2. Delwaide PJ: Contribution of human reflex studies to the understanding and management of the pyramidal syndrome, in Shahani BT (ed): Electromyography in CNS Disorders: Central EMG Boston, Butterworth, 1984, pp 77-111. 3. Delwaide PJ: Electrophysiologic testing of spastic patients: its potential usefulness and limitations, in Delwaide PJ, Young RR (eds): Clinical Neurophysiology in Spasticity. Amsterdam, Elsevier, 1985. 4. Denny-Brown D: The Cerebral Control of Movement. Liverpool, Liverpool University Press, 1966. 5. Gossman MR, Sahrmann SA, Rose SJ: Review of length-associated changes in muscle. Experimental evidence and clinical implications. Phys Ther 1982; 62:1799-1808. 6. Herman R: The myotatic reflex: clinico-physiological aspects of spasticity and contracture. Brain 1970; 93:273-312. 7. Herman R, Freedman W, Meeks S: Physiological aspects of hemiplegic and paraplegic spasticity, in Desmedt JE (ed): New Developments in Electromyography and Clinical Neurophysiology: Human Reflexes, Pathophysiology of Motor Systems, Methodology of Human Reflexes. Basel, Karger, 1973, pp 579-589. 8. Hoefer PFA, Putnam TJ: Action potentials of muscles in “spastic� conditions. Arch Neurol Psychiat (Chicago). 1940; 43:1-22. 9. Hufschmidt A, Mauritz KH: Chronic transformation of muscle in spasticity: a peripheral contribution to increased tone. J Neurol Neurosurg Psychiatry 1985; 48:676-685. 10. Katz RT, Rymer WZ: Spastic hypertonia: mechanisms and measurement. Arch Phys Med Rehabil 1989; 70:144-155.
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11. Knuttson E: Analysis of gait and isokinetic movements for evaluation of antispastic drugs and physical therapies, in Desmedt JE (ed): Motor Control Mechanisms in Health and Disease. New York, Raven Press, 1983, pp 1013-1034. 12. Kuypers HGJM: Anatomy of the descending pathways, in Brooks VB (ed): Handbook of Physiology. Bethesda, American Physiological Society, 1981. 13. Lance JW: Symposium synopsis, in Feldman RG, Young RR, Koella WP (eds): Spasticity: Disordered Motor Control Chicago, Year Book Medical Publishers, 1980. 14. Lance JW: Pyramidal and extrapyramidal disorders, in Shahani DT (ed): Electromyography in CNS Disorders: Central EMG. Boston, Butterworth, 1984, pp 1-19. 15. Mayer N, Esquenazi A, Childers MK: Common patterns of clinical motor dysfunction. Muscle Nerve 1997; 20 (suppl 6):S21-S35. 16. Nathan P: Some Comments on Spasticity and Rigidity, in Desmedt JE (ed): New Developments in Electromygraphy and Clinical Neurophysiology. Basel, Karger, 1973; pp 13-14. 17. Pierrot Deseilligny E, Mazieres L: Spinal mechanisms underlying spasticity, in Delwaide PJ, Young RR (eds): Clinical Neurophysiology in Spasticity. Amsterdam, Elsevier, 1985. 18. Rack PMH: The behavior of mammalian muscle during sinusoidal stretching. J Physiol London. 1966; 183:1-17. 19. Sahrmann SA, Norton BJ: The relationship of voluntary movement to spasticity in the upper motor neuron syndrome. Ann Neurol 1977; 2:460-465. 20. Schwindt PC: Control of motorneuron output by pathways descending from the brain stem, in Towe AL, Luschei ES, (eds): Handbook of Behavioral Physiology, vol. 15, Motor Coordination. New York, Plenum Press, 1981.
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21. Sherrington CS: Decerebrate rigidity and reflex coordination of movements. J Physiol London 1898; 22:319-322. 22. Sherrington CS: On plastic tonus and proprioceptive reflexes. Quart J Exp Physiol 1909; 2:109156. 23. Sherrington CS: Remarks on some aspects of reflex inhibition. Proc Roy Soc B 1925; 97:519545.
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