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Weakness in PatientsWith HemiparesisDaniel Bourbonnais,Sharyn Vanden NovenKey Words: brain injuries cerebrovasculardisorder. motor control musclecontraction. muscle strength

Clinical and experimental results are reviewedconcerning muscle weakness in patients with hemi-paresis after a stroke. The discussion includes theimportant role that alterations in the physiology ofmotor units, notably changes in firing rates andmuscle fiber atrophy, play in the manifestation ofmuscle weakness. This role is compared with thelesser role tha t spasticity (defined as hyperactivestretch reflexes) of the antagonist muscle group ap-pears to play in determining the weakness ofago-nist muscles. The contribution of otherfactors thatresult in mechanical restraint of the agonist by theantagonist (e.g., passive mechanicalproperties andinappropriate cocontraction) is discussed relative tomuscle weakness in patients with hemiparesis.

Daniel Bourbonnais, PhD, OTR, is Assistant Professor of Oc-cupational Therapy, Ecole de Readaptation, Universite deMontreal, Montreal, Canada H2E2C9.Sharyn Vanden Noven, PhD, PT, is Research Associate inthe Department of Anatomy, Medical College of Pennsylvania, Philadelphia. (Mailing address: 3200 Henry Avenue,Philadelphia, Pennsylvania 19129.)This article was accepted fo r publication january 12, 1989

The American journal of Occupational Therapy

Cerebrovascular accident, or stroke, is a common condition in patients seen by occupational therapists (Trombly & Scott, 1977;Walker, 1981). Initially, stroke results in hypotoniaand areflexia. The motor behavior usually progressesto a stage of spastic hemiparesis, which may include(a) spasticity, characterized by hyperactive stretch re-flexes, clonus, and the clasp-knife reflex; (b ) alter-ation of cutaneous reflexes (e.g., Babinski sign); (c )disturbance of other sensory functions (i.e., vision,proprioception, pain, temperature); and (d ) paresis.Paresis is a partial paralysis that is manifested by decreased muscle strength or weakness.

Clinically, muscle weakness has been recognizedby patients and therapists as a limiting factor (Duncan& Badke, 1987) in the motor rehabilitation of patientsafter a stroke. Muscle weakness is reflected by theinability of patients with spastiC hemiparesis to generate normal levels of muscle force. Deficits in "musclestrength" would reduce "the capacity of a muscle toproduce the tension necessary for maintaining pos-ture, initiating movement, or controlling movementduring conditions of loading of the musculoskeletalsystem" (Smidt & Rogers, 1982, p. 1283). Earlier re-views (Chan, 1986; Chapman & Wiesendanger, 1982;Pierot-Deseilligny, 1983) have focused on the issue ofspasticity and its role in the motor control of patientswith spastic hemiparesis. This paper reviews physio-logical changes in the nervous system of patients withhemiparesis that may contribute to muscle weakness.Normal Force ProductionA review of the physiology of normal force productionprovides the necessary background to understand thepossible mechanisms of muscle weakness in patientswith hemiparesis. (See Brooks, 1986, an d Evarts,Wise, & Bousfield, 1985, for a more detailed review.)

The force produced by a normal muscle contrac-tion depends on the number and type of motor unitsrecruited and the characteristics of that motor unitdischarge. In motor control, the motor unit represents the smallest functional unit. A motor unit comprises the alpha-motoneuron, its axon, and the musclefibers it innervates. (The term muscle unit may beused in reference to the muscle component of themotor unit.)Muscle force or tension is increased when eitherth e absolute number of active motor units is in-creased, or the firing rates of already-active motorunits are increased, or both (see Burke, 1981; Henneman & Mendell, 1981) Usually, both processes occursimultaneously. Motoneurons are organized in such away that the excitability of the motoneuron is responsive to the reqUired muscle unit force. Thus, an or-derly recruitment pattern of motor units on the basis

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of their force-producing characteristics exists inmovement. According to this principle, low-forceproducing motor units are the first to be recruited,and as force requirements increase, higher force-producing motor units are recruited. For example, in thetask of putting on a shirt, a certain number of motorunits in the agonist would be active. If, however, resistance was encountered, as in trying to move thehand through a small armhole, more and larger unitswould be recruited to meet the increased force demands. As force requirements for a movement decrease, motor units are derecruited in the reverseorder, with the higher force-producing units beingthe first to stop firing an d the low-foree-producingunits the last to stop firing. The central nervous system appears to match the amount of muscle forceproduced with the demands of the task. In general,low-threshold motor units (those recruited first) havesmaller motoneurons and axons and show less terminal branching than do high-threshold motor units.

Considering the full range of motor units innervating a given muscle, the motoneurons show a rangeof intrinsic properties and the muscle units show arange of histological and metabolic properties. Theunique properties of both motoneuron and musclecomponents of motor units are adapted to the orderlyrecruitment of motor units. Low-threshold motorunits, which develop less active force, are more resistant to fatigue than are high-threshold units. Motorunits are classified as type FF, FR, or S, on the basis ofthe fatigue resistance and twitch tension of the motorunits (Burke, 1981). Type FF refers to fast-contracting, fast-fatigUing motor units that can generate hightwitch tension. Such units are prevalent in musclesthat subserve fine movements of the hands and face.Type FR refers to fast-contracting but fatigue-resistantmotor units, and type S refers to fatigue-resistant,slow-contracting (meaning the twitch is long-lasting)motor units that generate low-twitch tensions. Type Smotor units are most prevalent in postural muscles.The succession of recruited motor units, from type Sto FR to FF, helps to provide for a smooth increase inthe force development.

Besides changes in the absolute number of activemotor units and the recruitment order of these units,muscle force is adjusted by changes in the firing ratesof the active motOr units. Each time the motoneuronfires, its muscle fibers contract, producing a singletwitch contraction. As the motoneuron firing rate increases, the individual muscle twitches summate toproduce more force output. This process continuesuntil the motor unit's level of maximal force output isachieved. The relationship between the stimulus rateof the muscle nerve and the force production in themuscle (i.e., a sigmoid, or S-shaped, relationship[Rack & Westbury, 1969]) defines an optimal range of

firing rates for motor units, over which an increase inthe firing rate results in an increase in the force production of the motor unit. Below this optimal range,the decreased firing of the motor unit will generateunfused twitches resulting in a small proportion ofthe motor unit'S force-generating capability. Abovethis optimal range, the increased firing of the motorunit cannot produce more tension because thetwitches had fused previously at an earlier rate to produce the unit's maximal tension. As with the order ofmotor unit recruitment, modifications in the firingrates of motor units can proVide fine gradations offorce, as observed in movements of the fingers or eyesthat are produced by muscles with a small number ofmotor units (Brooks, 1986). In these muscles that donot have a large number of motor units to recruit andderecruit, force development is graded more often bychanges in the firing rates of the available motor units.Physiological Changes in the HemipareticMotor SystemSpecific changes at the motoneuron or muscle levelcan decrease a person's ability to produce force,which will be observed, measured, an d documentedclinically as muscle weakness. These changes, summarized below, have been observed in strokepatients:

1. Motoneuron Changes:Loss of motor unitsChanges in recruitment order of motor unitsChanges in firing rates of motor units

2. Nerve Changes:Changes in peripheral nerve conduction

3. Muscle Changes:Changes in morphological and contractileproperties of motor unitsChanges in mechanical properties of muscles

Reductions in the level of force generated by theagonist muscles (i.e., the prime movers) in patientswith hemiparesis may result from direct changes(e.g., changes in the physiology of agonist motorunits) or from indirect changes (e.g., an increasedmechanical restraint, active or passive) that are imposed by antagonist muscles which oppose the actionof agonists. In this section, we will review evidencefrom clinical studies as to how such physiologicalchanges may contribute to the phenomenon of weakness in patients with hemiparesis.Direct Changes ofAgonist Motor Units

Decreased number of agonist motor units. Thenumber of active motor units participating in small,controlled movements has been examined in patients

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with hemiparesis. McComas, Fawcett, Campbell, &Sica (1971) developed a method to estimate the number of functioning motor units in normal subjects.McComas, Sica, Upton, & Aquilera (1973) then usedthis method with hemiparetic subjects. Between the2nd and 6th month after a stroke, the number of functioning motor units was reduced by approximatelyhalf. On e explanation for this loss is that degenerationof the corticospinal tract after a stroke results in transynaptic changes in the motoneurons (Dietz, Ketelsen, Berger, & QUintern, 1986; McComas et al., 1973).Changes in motoneuron properties could reduce theoverall activity of motor units as well as alter thefunction of their respective muscle unit components.

Denervation potentials (e,g., fibrillation and positive sharp waves) have been reported in hemipareticlimbs, indicating that some muscle fibers or muscleunits have lost connection with their motoneurons.Fibrillation potentials have been observed in abouttwo thirds of patients with hemiplegia and are recorded more often in distal muscles (Goldkamp,1967). This latter observation coincides with a possible role for the corticospinal tract in the denervationprocess, because this pathway projects more heavilyonto motoneurons supplying distal limb muscles(Kuypers, 1981). Other electromyographic studieshave confirmed the presence of a denervation processin patients with hemiparesis (Bhala, 1969; Cruz-Martinez, 1984; Johnson, Denny, & Kelley, 1975; Krueger& Waylonis, 1973; Segura & Sahgal, 1981; Spaans &Wilts, 1982). Alternatively, the appearance of denervation potentials in hemiparetic muscles could also beexplained by chronic pressure being exerted on peripheral nerves (Chokroverty & Medina, 1978). However, pressure blocks would also result in a decreasein the motor conduction velocity (maXimum) of peripheral nerves in patients with hemiparesis. Moststudies have not found such a result (Goldkamp,1967; McComas et al., 1973; Namba, Schuman, &Grob, 1971; Segura & Sahgal, 1981; Young & Mayer,1982); however, a few have (Cruz-Martinez, 1984;Panin, Paul, Policoff, & Eson, 1967). Indirect evidence supports the theory that some degenerativechanges of motoneurons may occur after a stroke;however, anatomical evidence for degenerativechanges in motoneurons (e.g., cell shrinkage, loss ofsynapses) after a stroke has no t yet been demonstrated in humans.

Changes in the properties ofagonist motor units.Muscle atrophy is a common clinical finding in patients with hemiparesis. Evidence on fiber measurements in biopsied muscle supports the idea that thepresumptive fast-contracting fibers belonging tohigh-threshold motor units (type FF or FR, higherforce producing) are atrophied in patients with hemiparesis (Brooke & Engel, 1969; Dietz et al., 1986;

The American journal oj Occupational Therapy

Edstrom, Grimby, & Hannerz, 1973; Scelsi, Lotta,Lommi, Poggi, & Marchetti, 1984). Hypertrophy ofpresumptive slow-contracting muscle fibers belonging to low-threshold (type S, low-force-producing)motor units has also been reported (Edstrom, 1970).Such modifications of the morphological characteristics of muscle in general, and of muscle units in particular, could alter the force-producing capability ofmotor units.Studies on the contractile properties of motorunits in patients with hemiparesis have shown that theoverall contraction time is prolonged in hemipareticmuscle (McComas et al., 1973; Visser, Oosterhoff,Hermans, Boon, & Zilvold, 1985). In particular, themean twitch contraction time is increased in fast-contracting motor units (Young & Mayer, 1982). Furthermore, a unique class of motor units-slow-contracting and fatigable-not present in normal muscle,have been found in long-term hemiparetic muscle.Young and Mayer found, in general, that all motorunits recorded from the paretic side of patients withhemiparesis were more fatigable, as judged by a fa-tigue index (i.e., the ratio of twitch tension before andafter a repetitive stimulus train). In the clinic, theincreased fatigability of the hemiparetic motor systemwould be reflected by a patient's poor endurance inperforming repetitive tasks or movements.Disrupted recruitment order of agonist motOrunits. To date, there is conflicting evidence as towhether the recruitment order of motor units isdisrupted in patients with hemiparesis. An early observation of abnormal recruitment order of motorunits in patients with hemiparesis (Grimby, Hannerz,& Ranlund, 1972; Grimby & Hannerz, 1973) has notbeen confirmed (Rosenfalck & Andreassen, 1980).Such studies, which require the sampling of motorunits across the full range of activation thresholds,have been limited by the recording technology. In thefuture, tungsten electrodes (Bigland-Ritchie, 1983),which offer selective recording of high- and lowthreshold motor units in human muscle, may allow fora more definitive evaluation of the recruitment pattern of motor units in patients with hemiparesis.Decreased agonist motor unit firing rates. If theoverall firing rates of motor units are decreased inpatients with hemiparesis, then the active motor unitswill generate less effective tension (Rack & Westbury,1969). Consequently, for a patient to reach a givenforce level or to produce a particular movement, additional m otor units would have to be recrUited. Thisexplanation would account for the increased levels ofelectromyographic activity pe r unit of force observedin elbow flexor muscles of paretic limbs, comparedwith contralateral nonparetic limbs in a subpopulation of patients with hemiparesis (Tang & Rymer,1981). Similar results have been reported for other

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muscle groups of upper and lower limbs (Visser &Aanen, 1981), Also, Freund, Dietz, Wita, & Kapp(1973) showed a decreased firing rate in motor unitrecordings from intrinsic hand muscles of patientswith hemiparesis. A similar decrease was observed(Rosenfalck & Andreassen, 1980) in the mean firingrate of motor units recorded from the tibialis anteriormuscle of patients with hemiparesis. However, in another study (Dietz et al., 1986), no difference wasfound between the mean firing rates of gastrocnemiusmotor units recorded from affected and unaffectedsides of patients with hemiparesis. More studies areneeded to elucidate this important point, because anoverall decrease in the firing rates of motor units inparetic muscle would directly contribute to muscleweakness (Rosenfalck & Andreassen; Tang & Rymer).Peripheral feedback may help to maintain a constant force level in the modulation of motor unit firingfrequencies. When a patient with hemiparesis tries tomaintain a constant force level, th e force recordshows irregularities not observed in normal subjects(Rosenfalck & Andreassen, 1980). Difficulty in maintaining a constant force level could be important forthe performance of finely controlled movements suchas writing or eating. In patients with hemiparesis, theinability to maintain a constant force level has beenrelated to a problem in the modulation of motor unitfiring frequencies. Rosenfalck & Andreassen pro-posed that this deficit may indicate a disturbance inthe usage of peripheral feedback for the control ofhemiparetic movement. Overall, changes observed inhemiparetic muscles suPPOrt the idea that the agonistmotor units themselves have been altered. An understanding of the specific mechanisms responsible forthese changes will require further research.

Passive or Active Restraint ofAgonist ActivationAny alteration in the motor system that constrains,either by a passive or active process, the contraction ofthe agonist limits the patient's ability to produce effi-cient voluntary movements. This concept was recognized in the treatment of patients with spastic hemiparesis by Bobath (1978), who suggested that weakness in the agonist results from spasticity (defined byhyperactive stretch reflexes) of the antagonist muscle.Considering the possible link between agonist muscle dysfunction and antagonist muscle spasticity, Bobath proposed that the normalization of muscle toneis a priority for the rehabilitation of these individuals.The idea is that a reduction or elimination of the spasticity would unmask the voluntary capabilities of thepatient for movement.

Recent evidence in patients with hemiparesis,however, does not support a major role for the spastic

ity of the antagonist in limiting voluntary activation ofthe agonist. Bohannon, Larkin, Smith, & Horton(I987) reported that a measure of decreased musclestrength in the upper limb musculature of patientswith hemiparesis correlated with the level of spasticity assessed in these same muscles, but not with thelevel of spasticity in the antagonists. The covariationbetween the level of spasticity and the measure ofstrength for the agonist muscle group would not beexpected if the spasticity of the antagonist muscleswere responsible for the observed decrease in agonistmuscle strength, However, in Bohannon et al. (1987),the low incidence of spasticity in the antagonist muscle group across subjects does not proVide a definitivetest of its role in limiting voluntary activation of theagonist.

Passive mechanical restraint of agonist activa-tion. Studies that examine the increased resistance ofspastic-paretic muscle to externally imposed stretchprovide a means to assess contributions from reflexand mechanical (structural) factors. In a study by Lee,Broughton, & Rymer (1987), four patients with spastichemiparesis who demonstrated increased resistancein elbow flexor muscles to externally imposed stretch(i.e., spasticity) on the paretic side as compared withthe contralateral side also showed low electromyographic activity in the paretic muscles (i.e., flexorsand extensors). Therefore, the measured resistance ofthe limb to passive stretch was not due to enhancedstretch reflexes. Lee et al. concluded that the increased resistance to stretch was due to altered mechanical properties of the elbow musculature in thesepatients with hemiparesis.

Other studies (Dietz, Quintern, & Berger, 1981;Hufschmidt & Mauritz, 1985) supported the importance of mechanical properties over stretch reflex enhancement in limiting voluntary activation of muscles. During th e SWing phase of gait, Dietz et al.(1981) found that difficulty in dorsiflexing the spastic-paretic foot was accompanied by a significant increase in the electromyographic activity in the tibialisanterior muscle, as compared with normal subjects.Because no coactivation of the triceps surae muscles(antagonists) was observed, Dietz et al. (1981) proposed that the excessive activation of the tibialis anterior muscle was necessalY to overcome a resistance ofnonreflexive origin (e.g., some alteration in the passive mechanical properties of the triceps surae musclegroup). likeWise, results of Hufschmidt and Mauritz,in characterizing the passive mechan ical properties ofspastic ankle muscles in patients with hemiparesiswith longterm spasticity, supported the hypothesisthat structural changes occur in spastic muscle.

Active restraint of agonist activation. Inappropriate activation of antagonist muscles during a movement that requires selective activation in the agonist

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muscle group would limit the force generated by theagonists. Abnormal patterns of muscle activation inpatients with hemiparesis are manifested by their difficulty in controlling the temporal relationship ofagonist/antagonist muscle pairs. This includes theability to activate as well as to deactivate muscles producing a motion, for example, the rapid alternatingmovements necessary to brush teeth or to write.

In normal persons, both postural (Keshner,Allum, & Pfaltz, 1987) and voluntary (Smith, 1981)movements are executed by the coactivation of agonist/antagonist muscles acting at a single joint. Coactivation, or cocontraction, itself is not an abnormalphenomenon in motor control. However, in subjectswith hemiparesis, inappropriate, ungraded cocontractions of agonist/antagonist muscles have beendemonstrated in gait (Conrad, Benecke, & Meick,1985; Dietz et aI., 1981; Knutsson, 1985; Knutsson &Richards, 1979), in dynamic movements (Angel,1975; Knutsson & Martensson; 1980, Sahrmann &Norton, 1977), and under static conditions (Berardelli, Accornero, Hallet, Innocenti, & Manfredi,1985). The motor problems produced by these inappropriate, ungraded cocontractions may be more limiting to active movements than to passive movements.Investigators have found that the restraint imposed byantagonist muscles is low during passive movementsbut higher during voluntary movements performed atthe same speed (Knutsson & Martensson; Mclellan,1977). This suggests that for active movements, inappropriate, ungraded cocontractions of antagonistsmay limit agonist force production.

In summary, studies to date do not support amajor role for the spasticity of the antagonist in limiting the production of agonist muscle force Agonistmuscle dysfunction in patients with spastic hemiparesis may be due more to restra int factors imposed bythe passive mechanical properties of antagonist muscles and surrounding tissues and/or by inappropriate,ungraded cocontractions of antagonists.

Clinical Significance ofMuscle Weakness inHemiparesisIt is questioned whether the terms muscle weaknessand muscle strength apply to people with spasticity.Muscle weakness usually refers to less-than-normalmuscle strength. I f so, then a patient with hemiparesiswho demonstrates weakness of the upper limb musculature could benefit from a regimen of strengthening exercises. To se t up such a program, baseline datamust be obtained to assess the patient's initial level ofmuscle strength. However, strength training andstrength measurement testing to monitor motor statusand recovery after a stroke are controversial issues.

The Americanjournal of Occupational Therapy

The assessment of true muscle strength can be confounded by severe spasticity, abnormal passive mechanical properties of muscles, or abnormal muscleactivation patterns (e.g., cocontraction). However, ifthe ability to produce an efficient muscle contractionis the basis for any movement (Duncan & Badke,1987), then as therapists, we must rethink the potential merit of strengthening exercises for our patientswith hemiparesis. We must consider conditions inwhich paretic muscle can be strengthened to helprather than to hurt the patient. Clinical studies canhelp us with this consideration.

Ineffective muscle contractions reduce forceOutput in patients with hemiparesis (Bourbonnais,Vanden Noven, Carey, & Rymer, 1987, in press),thereby affecting all movements and limiting functional performance. Overall, the maximal force produced by a given muscle group on the paretic side isreduced in patients with hemiparesis (Rosenfalck &Andr,_assen, 1980; Visser et a1., 1985). Bohannon(1987) examined strength deficits (i.e, ratio of paretic to nonparetic muscle strength) in patients withhemiparesis and found that parameters such asgender, weight, and age, which correlated withstrength measures for normal or nonparetic muscles,did not correlate with strength measures for pareticmuscles. The impact of such disrupted relationshipson the functioning of the hemiparetic motor systemhas not been determined.

The inefficiency of muscle contractions in patients with hemiparesis was found to be related to themotor performance of the evaluated limb (lowerlimb: Badke & Duncan, 1983; upper limb: Bourbonnais et aI., 1987, in press), as assessed by the FuglMeyer test of motor performance (Fugl-Meyer,Jaasko,Leyman, Olsson, & Steglind, 1975). Other measuresof strength have been examined in patients withhemiparesis and considered as potential predictorsfor functional independence For example, Bohannon(1986) reported that improvement in muscle strengthin patients with hemiparesis was related to clinicalimprovement. Andrews, Brocklehurst, Richards, &Laycock (1981) reported that for patients 3 monthsafter a stroke, improvements in muscle strength coincided with improvements in the performance of activities of daily living. Bohannon & Smith (1987) foundthat their strength measures for paretic muscle groupsreflected an improvement in strength (estimated at20%) after 1 month of a rehabilitative program. Presumably, thiS improvement in strength was the netresult of any spontaneous central nervous system recovery (e.g., after decreased edema) or motor recovery due to the therapeutic exercise regime. More studies on patients with hemiparesis are reqUired to assesswhat role muscle strength training should play in rehabilitating patients after a stroke

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ConclusionPhysiological changes in th e motOr system of adultpatients with hemiparesis, which might account, inpart, for muscle weakness, have been reviewed. Suchchanges ar e often interrelated, and their effects summate, along with other factors, to contribute to theoverall severity of the motor disturbance. Fo r example, a patient's ability to produce muscle force can belimited by specific changes at th e motoneuron ormuscle level or by changes in the organization of thenervous system. For a more in-depth discussion of th emotOr control of stroke patients as well as for examples of ho w ou r present knowledge of motor control,on the basis of research findings, ca n be melded withthe clinical treatment approach, see Duncan andBadke (1987)

Further clinical research is required to sort outth e relative contributions of th e above-mentionedfactors to th e phenomenon of muscle weakness inpatients with hemiparesis. Both occupational andphysical therapists have considerable expertise tocontribute to the study of motor control problems.This is exemplified by th e groWing number of therapist-researchers contributing to our knowledge basein normal and abnormal motor control.AcknowledgmentWe thank Dr. Emily Keshner for her thoughtful criticisms ofan earlier version of the manuscript.References

Andrews, K., Brocklehurst, G. c., Richards, B., & Lay-cock, P. J. (1981). The rate of recovery from stroke and itsmeasurement. International Rehabilitation Medicine, 31,155-161Angel, R. W. (1975). Electromyographic patterns during ballistic movement of normal and spastiC limbs. BrainResearch, 99, 387-392.Badke, M. B., & Duncan, P. W. (1983). Patterns of rapidmotor responses during postural adjustments when standing in healthy subjects and hemiplegic patients. PhysicalTherapy, 63, 13-20.Berardelli, A., Accornero, N., Hallet, M., Innocenti, P.,& Manfredi, M. (1985). EMG burst duration during fast armmovements in patients with the upper motor neurone. InP. J. Delwaide & R. R. Young (Eds.) , Clinical neurophysiology in spasticity (pp. 77-82). Amsterdam: Elsevier.Bhala, R. P. (1969). Electromyographic evidence oflower motor neuron involvement in hemiplegia. Archives ofPhysical Medicine and Rebabilitation, 50, 632-641.Bigland-Ritchie, B. (1983). Changes in motoneuronefiring rates during sustained maximal voluntary contractions. journal of Physiology, 340, 335-346.Bobath, B. (1978). Adult henuplegia: Evaluation andtreatment. London: William Heinnemann.

Bohannon, R. W. (1986). Strength of lower limb related to gait velocity and cadence in stroke patients. Physiotherapy Canada, 38, 204-206.Bohannon, R. W. (1987). Relationship between staticstrength and various other measures in hemiparetic stroke

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Bohannon, R. Wi' Larkin, P. A., Smith, i\1. B., & Horron,M. G. (1987). Relationship between static muscle strengthdeficits and spasticity in stroke patients with hemiparesis.Physical Therapy, 67, 1068-1071Bohannon, R. Wi., & Smith, M. B. (1987). Assessment of

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Bourbonnais, D., Vanden Noven, S., Carey, K., &Rymer, W. Z. (1987). Patterns of muscle activity during isometric contractions in spastic hemiparesis. Society forNeurosc ience Abstracts, 12, 1304.

Bourbonnais, D., Vanden Noven, S., Carey, K., &Rymer, W. Z. (in press). Abnormal patterns of elbOW muscleactivation in hemiparetic subjects. Brain.Brooke, M. H., & Engel, W. K. (1969). The histographicanalysis of human biopsies with regard to fiber types: 2.Diseases of upper and lower motor neurons. Neurology, 19,378-393Brooks, V. B. (1986). The neural basis of motor control. New York: Oxford University Press.Burke, R. E. (1981). Motor units: Anatomy, physiologyand functional organization. In V. B. Brooks (Ed.), Hand-book of Physiology: The nervous system: Vol. 2. Motor control (pp. 345-422). Bethesda, MD: American PhysiologicalSociety.Chan, C. W. Y. (1986). Some techniques for the reliefof spasticity and their physiological basis. PhysiotherapyCanada, 38, 85-89.

Chapman, E., & Wiesendanger, M. (1982). The physiological and anatomical basis of spasticity: A review. Physiotherapy Canada, 34,125-136.Chokroverty, S., & Medina, J. (1978). Electrophysiological study of hemiplegia. Archives of Neu.rology, 35,360-363.Conrad, B., Benecke, R., & Meick, H. M. (1985). Gaitdisturbances in paraspastic patients. In P. J. Delwaide &R. R. Young (Eds.), Clinical neurophysiology in spasticity(pp. 155-174). Amsterdam: Elsevier.Cruz-Martinez, A. (1984). Electrophysiological studyin hemiparetic subjects: Electromyography, motor conduction and response to repetitive nerve stimulation. Electroencephalography and Clinical Neurophysiology, 23,139-148.Dietz, V., Ketelsen, U. P., Berger, W., & Quintern, J.(1986). MotOr unit involvement in spastic paresis: Relationship between leg muscle activation and histochemistry.journal ofNeurological Sciences, 75, 89-103.Dietz, V., Quintern, J., & Berger, W. (1981). Electrophysiological studies of gait in spasticity and rigidity: Evi-dence that altered mechanical properties of muscle contribute to hypertonia. Brain, 104,431-449.Duncan, P. W., & Badke, M. B. (1987). Stroke rehabilitation: The recovery of motor control. New York: YearBook.Edstrom, L. (1970). Selective changes in the sizes ofred and white muscle fibers in upper motor lesions andParkinsonism. journal oj Neurological Sciences, 11,537-550.Edstrom, L., Grimby, L., & Hannerz,J. (1973). Correlation between recruitment order of motor units and muscleatrophy pattern in upper motoneurone lesion: Significanceof spasticity. Experimentia, 29, 560-561.Evarts, E. W., Wise, S. P., & Bousfield, D. (1985). Themotor system in neurobiology. Amsterdam: Elsevier.

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Freund, H.]., Dietz, V., Wita, C. W., & Kapp, H. (1973).Discharge characteristics of single motor units in normalsubjects and patients with supraspinal motor disturbances.In]. E. Desmedt (Ed.), New developments in electromyography and clinical neurophysiology (pp. 242-250). NewYork: S. Karger.Fugl-Meyer, A. R., jaasko, L., Leyman, I. , Olsson, S., &Steglind, S. (1975). The post-stroke patient: A method ofevaluation of physical performance. Scandinavian journalofRehabilitation Medicine, 7, 13-31.. Goldkamp, 0 (1967). Electromyography and nerveconduction studies in 116 patients with hemiplegia. Archives ofPhysical Medicine, 48, 59-63.Grimby, L., & Hannerz, ]. (1973) Tonic and phasic

recruitment order of motor units in man under normal andpathological conditions. In j. E. Desmedt (Ed.) , New developments in electromyography an d clinical neurophysiology (Vol. 3, pp. 225-233). New York: S. Karger.Grimby, L., Hannerz, ]., & Ranlund, T. (1972). Disturbances in the voluntary recruitment order of anterior tibialmotor units in spastic paraparesis upon fatigue. journal ofNeurology, Neurosurgery and Psychiatry, 37, 40-46.

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