Principles of Force Gradation in Skeletal Musclesdownloads.hindawi.com/journals/np/2003/858709.pdf · muscle force during motor behavior. Basic properties of motoneurons and muscle

NEURAL PLASTICITY VOLUME 10, NO. 1-2, 2003

Principles of Force Gradation in Skeletal Muscles

D. Kemell

Department ofMedical Physiology, University ofGroningen, Groningen, The Netherlands

ABSTRACT

A brief survey is given of how motoneuronsand motor units are used for the gradation ofmuscle force during motor behavior. Basic

properties of motoneurons and muscle fibers,including major kinds of functional specializationalong the axis of ’fast’ vs. ’slow’, are reviewed.The principles underlying the rate and recruit-ment gradation of force are described, stressingthat the properties of motoneurons and musclefibers are matched to automate importantaspects of the gradation procedure. Recentinvestigations concerning synaptically evokedchanges in the discharge properties of moto-neurons receive special attention, including’plateau’ currents and, under appropriateconditions, self-sustained ’plateau’ discharges.

KEYWORDS

motoneurons, muscle units, recruitment gradation,rate gradation, plateau currents

INTRODUCTION

The deficient coordination of a clumsy child

means, purely descriptively, that the child’s bodyis not moving around in the most optimal manner.

Reprint requests to: D. Kernell, Department of MedicalPhysiology, University of Groningen, PO Box 196, 9700 ADGroningen, The Netherlands; e-mail: [email protected]

Thus, the many muscles involved are not

contracting at the most optimal force levels for themotor task. Most of this problem is likely to becaused by dysfunctions of ’high’ brain mechanisms

(for example, in neocortex, basal ganglia, cerebellum,brainstem). Nevertheless, motor programs and plansat these higher levels have, ultimately, to becomeshaped into motor behavior via commands to thefinal common path of the motor system: themotoneurons and the muscle fibers. Thus, whateverthe characteristics of the motor behavior, whetherclumsy or not, the motor output system is alwaysinvolved. As a background for further discussionsabout the mechanisms of motor function anddysfunction, I give here a brief survey of how theoutput machinery is organized and how it works, ata cellular level and under normal conditions (forgeneral reviews, see Burke, 1981; Henneman &Mendell, 1981; Kemell, 1992; Binder et al., 1996).

WHAT IS CONTROLLED? STRUCTURALORGANIZATION OF MOTONEURONS AND

MUSCLE FIBERS

Anatomists have enumerated and named severalhundred ’muscles’ in the body. In fact, from a

functional point of view, the number of distinct

force-producing units is even larger than it seems

from textbooks because many of the anatomical’muscles’ consist of several different portions thatexert their forces in different directions. A clearexample of this is, for instance, the deltoid muscleat the shoulder joint. The force-generating cellswithin a muscle are the long and threadlike skeletal

(C) 2003 Freund & Pettman, U.K. 69

70 D. KERNELL

muscle fibers, which are often around 50 gm thickbut several thousand microns long. Each musclefiber receives innervation from a motoneuron, a

specialized nerve cell having its cell body anddendrites inside the central nervous system andsends its axon into the periphery. Inside a targetmuscle, the motor axon splits up into numerousterminal branches. Thus, a single motoneurontypically makes synaptic contact with many musclefibers, whereas each single muscle fiber receivesinnervation from only one motoneuron. Amotoneuron with its muscle fibers constitutes one’motor unit’, and the muscle fibers of a motor unitare often also collectively called a ’muscle unit’.Within skeletal muscles, muscle fibers of differentunits are intermingled.

Muscle fibers normally contract only whenexcited by their motoneuron. The muscle unit is thesmallest fraction of a muscle that can be activatedby the central nervous system. Each muscle iscontrolled by a population of motoneurons, a’motoneuron pool’. The cell bodies of the moto-neurons lie in the ventral horn of the spinal cord or,for those of cranial nerves, within nuclei of the brainstem. In the spinal cord, the motoneurons of singlemuscles are organized into elongated cell groups.

The axon terminations of a single motoneuronare typically restricted to a single muscle (only afew exceptions from this rule are known; Emonet-Denand et al., 1971; Sekiya et al., 1992) or even, inseveral known cases, to distinct portions within

single muscles (neuromuscular compartments; forexample, English & Letbetter, 1982). Thus, centralmechanisms are almost always needed for theactivation of different muscles together, as requiredfor coordinated motor behavior.

DIFFERENTIATION OF MUSCLE FIBERPROPERTIES IN RELATION TO MOTOR TASKS

An activated muscle produces a force in a

shortening direction; muscles are used for pulling

on things, not for pushing. Besides producingmovements by means of muscle shortening(concentric contractions), practically all musclesare also used for ’postural’ tasks (namely, forstabilizing joints, often near-isometric contractions)and for ’braking’ tasks (lengthening or eccentric

contractions). Different kinds of motor tasks are

associated with different mechanical, metabolic,and circulatory conditions, and different musclefibers have become specialized accordingly.

The fact that at all muscle fibers are not alikeis easily demonstrated by staining a cross-sectionof a muscle for its contents of various kinds ofenzymes or contractile proteins. Using standardprocedures for the staining of a constituent of themyosin molecule, the myofibrillar ATPase(mATPase), two main fiber categories are generallyclearly revealed, referred to as type and II (lightand dark respectively after alkaline preincubation).Within each single muscle unit, the various musclefibers typically have very similar physiologicaland biochemical properties; thus, from this pointof view, muscle units tend to be functionallyhomogeneous. Hence, the muscle units can also beclassified as belonging to different functional types.

The results of combined physiological andhistochemical studies have demonstrated that typeI fibers tend to be slow and highly resistant to

fatigue; thus, they can keep up a series of repeatedcontractions with little loss of force. At the otherextreme, type II fibers are fast but more fatigable;typically, this group is subdivided into several

subgroups. In experimental physiological studies,Burke’s (1981) scheme of unit classifi-cation is

often used, categorizing the units into the majorgroups of (a) fast-twitch fatigue-sensitive (FF),(b) fast-twitch fatigue-resistant (FR), and (c)slow-twitch fatigue-resistant (S).

The shortening contractions that we need forthe production of movements might have to be

performed rapidly and at great power; in theseinstances muscles can be activated to the extent

FORCE GRADATION IN SKELETAL MUSCLES 71

that circulation is temporarily rendered ineffectivebecause of pressure on blood vessels fromcontracting muscle fibers. Correspondingly, the Funits are good at rapidly getting energy out ofintramuscular glycogen stores, even withoutimmediate access to oxygen.

Postural contractions are often near-isometricand relatively weak but sometimes have to bemaintained for very long times, up to hours.Correspondingly, the muscle fibers of S units havea high degree of endurance; they are well providedwith enzymes for oxidative metabolism and are

also surrounded by many capillaries for thecontinuous supply of oxygen and fuel and removalof waste products. The ’slowness’ of these fibersmakes them metabolically cheap to use in long-lasting near-isometric contractions.

GRADATION OF CONTRACTILE FORCE:RATE AND RECRUITMENT CONTROL

Rate gradation of single unit force

The force-producing muscle fibers of our

muscles are the so-called ’twitch fibers’, activated

via the generation of action potentials. Each timean action potential comes along a motor axon, the

potential is transmitted across the neuromuscularsynapse at all its muscle fibers. Within each musclefiber, the action potential is propagating all along its

length, activating contractile mechanisms.The contraction caused by a single action

potential is referred to as a twitch, the smallest andshortest possible contraction caused by the neuronalactivation of a muscle unit. The twitch lasts much

longer than the action potential, but it is still too

brief for normal motor behavior. Practically all

kinds of movements are evoked by trains of

repetitive action potentials. If such a train occurs

with action potential intervals similar to the twitch

duration, we will simply see a repeated series of

twitches. If the action potential rate is increased,the twitches seem to ’summate’" they grow intoeach other and peak force becomes increased.Thus, over a given range of spike-frequencies, anincreased action potential rate gives an increasedforce; this is how force is graded in single musclefibers and muscle units. Above a given rate, thisprocess saturates. Then the twitches are completely’fused’, and a further increase of action potentialrate gives no increase of force.

Muscles react differently under differentconditions. Their force production is influenced bymuscle length and by shortening velocity. Further,for the same activation pattern, force may increase

(’potentiation’) or decrease (’fatigue’) as a resultof after-effects of preceding activity. The rate-

gradation of force is also influenced by muscletemperature and by the precise pattern of pulseintervals in the activation train (review: Binder-

Macleod, 1992). However, under each set ofconditions, the relation between contractile forceand stimulation rate (’tension-frequency’ or ’T-f’curve) has, as far as we know, essentially the same

general shape" a sigmoid curve with a rathernarrow frequency-range within which a variation

in activation rate also gives an effective alteration

of contractile force. This is the frequency range(with some variation, depending on the

circumstances) within which motoneurons have to

operate for the effective gradation of force in

single units. This is also roughly the frequencyrange within which motoneurons are often actuallyfound to operate. How is this controlled?

Rate modulation of single motoneuronal activity

A single motoneuron receives thousands of

synapses from other cells along its extensive

dendritic trees. The discharge activity of a moto-

neuron is controlled by the summed excitatory and

inhibitory activity of all these synapses. Each

single synapse produces only a very small effect.

72 D. KERNELL

For the production of impulse discharges in a

motoneuron, many excitatory synapses have to beactive more or less simultaneously. If the summedpostsynaptic current is sufficiently strong andlong-lasting, then the motoneuron reacts bygenerating a repetitive impulse discharge. Thisprocess can be imitated by applying currents ofdifferent intensity to a single motoneuron via amicroelectrode. In this way, one can determinehow the motoneuron translates current intensityinto impulse frequency (’frequency-current’ or ’f-I’relation). Over an important lower portion of thetotal frequency-range of a motoneuron, a practicallylinear relation exists between the discharge rateand current. For a given motoneuron, this linear

’primary range’ of discharge corresponds fairlywell to the steep portion of the T-f curve for itsmuscle fibers. Thus, motoneurons have membraneproperties that cause them automatically todischarge at rates that are optimal for the gradationof force in their muscle fibers. For such matching,no controlling neuronal machinery is required. Thematching also works across the various types of Sand F muscle fibers. Because of their intrinsic

membrane properties, the motoneurons of S fibersare active within a lower frequency range than thatfound for motoneurons of F fibers.

Recruitment control in motoneuron populations

So far I have dealt only with the rate gradationof force in single muscle units. Muscles are not

run by single motoneurons, however, but rather bypopulations of often tens or hundreds of moto-

neurons. Thus, as one might predict, muscle forceis also varied by activating smaller or larger numbersof motoneurons. This phenomenon is referred to as

the ’recruitment gradation’ of force.Many synaptic inputs to functional populations

of motoneurons (for example, those of a singlemuscle) are organized such that single premoto-

neuronal axons send branches to many (or even to

all) motoneurons involved. Thus, an increasedincoming excitation will practically always go to a

substantial portion of the motoneuron poolsimultaneously: if one motoneuron receivesexcitation, then its ’colleagues’ are likely toreceive it as well, although possibly in differentquantities. For the achievement of a useful recruit-ment gradation of force, the various motoneuronsshould not all be activated at the same thresholdlevel of input. This does not easily happen,however, because, due to differences in intrinsicmembrane properties, the motoneurons of a singlepool differ very much in their electrical excitability.These differences are such that the various typesof muscle units tend to be appropriately selectedfor different motor tasks.

In most studied kinds of voluntary or reflexcontractions, the weak, slow, and fatigue-resistantS units are those most easily recruited; these unitsare very suitable for producing the weak but long-lasting contractions that are necessary formaintaining and controlling posture. The strong,fast, and fatigue-sensitive FF units are recruited at

the other end of the threshold range, which seems

appropriate as these units are particularly adaptedto the production of the high-power but typicallyrelatively short-lasting contractions necessary fordriving rapid movements. This recruitment

hierarchyfrom weak and slow toward strongerand faster units---corresponds to the motoneuronaland motor unit behavior summarized in the term

’size principle’ described by Henneman and his

colleagues (review: Henneman & Mendell, 1981).Also in this case, the choices are largely made inan automatic manner, depending on the intrinsicexcitabilities of the respective motoneurons; no

complex neuronal circuitry is needed forgenerating these basic patterns of motoneuron poolbehavior. Until all motoneurons of a pool havebecome recruited, rate and recruitment gradationtend to be used more or less in parallel.


VARIATIONS IN THE BEHAVIOR OFINDIVIDUAL MOTONEURONS AND

MOTONEURON POOLS

So far I have given a textbook-like descriptionof how force is graded in skeletal muscles. Themanner in which the basic set of mechanisms isused, however, can change in various ways,depending on the motor task and the history of thesystem. Much of the current research concerns thisflexibility of the motor output machinery. Thefollowing are two major aspects"a. the recruitment gradation may take place in

different ways for different motor tasks becauseof differences in synaptic distribution acrossthe motoneuron population;

b. the rate and recruitment gradation characteristicscan become modified because of short- or long-term alterations in the functional properties ofindividual motoneurons.

Variations of motoneuron pool innervation

The ease with which a synaptic input to a

functional motoneuron pool may grade moto-neuronal recruitment depends on how close to

each other the activation thresholds for themotoneurons are lying. If they were close together,then small changes of pool input would cause largevariations in recruitment. On the other hand, if therecruitment thresholds were very far apart, thengradation would be difficult and strong synapticinputs might conceivably fail to recruit the wholemotoneuron population. The relative activation

thresholds within a motoneuron pool might bemarkedly altered by synaptic inputs. For instance,if a certain input gave relatively more excitation to

intrinsically less excitable motoneurons, then

functional recruitment thresholds would come

closer together and, hence, the ’recruitment gain’would become increased (Kemell & Hultborn,1990). Motoneurons receive their synaptic inputs

from many different sources, and it is very likelythat the organization of their total input mightshow a great variation across different motor tasks.Recruitment gain would be altered by variations insynaptic distribution along the axis of S <--> Fmotoneurons. Several studies in the past havedemonstrated the existence of such differences:some systems are biased toward the S or F side ofthe spectrum, other systems are S vs. F neutral (forexamples, Powers & Binder, 2001). Thus, it ishighly likely that changes in recruitment gain mayindeed take place during the course of normalmotor behavior.

A further complication concerns the extent towhich the various synaptic command systems are

targeted onto whole motoneuron pools. It has longbeen known that, depending on the motor patternto be executed, different ’task groups’ of units maybe preferentially activated within single muscles(Hoffer et al., 1987). Such groups may be localizedwithin topographically different muscle portions,each containing fast as well as slow muscle unit

types. Furthermore, this situation might occur alsoin cases for which contractions of these differentmuscle portions have very similar mechanicaleffectsfor example, long head of human bicepsbrachii (ter Haar Romeny et al., 1984), or cat’speroneus longus (Hensbergen & Kernell, 1992).An intriguing question is how such ’task groups’are organized in a multi-muscular context" are thetrue ’functional’ motoneuron pools, for a givensynaptic command system, consisting of fractions

from the pools of several anatomical muscles,bundled together for specific spatial patterns ofmuscle coordination?

Changes in the activation properties of individual

motoneurons

Recent investigations have revealed two majorclasses of synaptic influence on motoneuronaldischarges:

74 D. KERNELL

a. Excitatory or inhibitory synaptic activation canhave the conventionally expected effect of simplyproducing currents that alter the motoneuronaldischarge in accordance with its intrinsic f-Irelation. In anesthetized animals, activatedsynapses mainly provide such ’driving currents’.Thus, there is then often a relatively goodagreement between the effects of postsynapticcurrents and corresponding intensities of injectedcurrents (Granit et al., 1966; Kemell, 1969;Powers & Binder, 1995, 2000; 2001).

b. Much research is going on concerning post-synaptic effects of a ’motoneuron-modifying’kind. In this case, synapses do not provideonly excitatory or inhibitory currents but also(or mainly) alter the way in which moto-neurons respond to driving currents. The bestknown effect of this kind concerns a

modification of motoneuronal membraneproperties such that the motoneuron becomespartly ’self-stimulating’. Under such conditions,the motoneuronal membrane becomessensitized such that it generates a persistentinward current when depolarized above a

certain level during a sufficient length of time

(Delgado-Lezama & Hounsgaard, 1999;Heckman & Lee, 1999; Hultborn, 1999; cf.Schwindt & Crill, 1980). This self-generatedcurrent adds to any synaptically or externallysupplied excitation; thus, it will drasticallychange the rate gradation properties of themotoneuron. The self-generated persistentinward current (’plateau current’) is

predominantly mediated by L-type Ca++

channels. Once started, such a current maysometimes even suffice to let a motoneuroncontinue firing repetitively, even if thesynaptic excitation becomes interrupted(’plateau firing’).

With regard to motoneurons, the earliest publishedexamples of ’plateau-facilitating’ post-synaptic

effects included monoaminergic actions in cat

(noradrenalin, serotonin) and turtle (serotonin)spinal cord (for example, Hounsgaard et al., 1986).Since then, several other kinds of metabotropicreceptors have been found whose activation mayfacilitate the emergence of plateau currents

(Delgado-Lezama & Hounsgaard, 1999).In addition to facilitating the emergence of

plateau currents, motoneuron-modifying synapsescan also cause a decrease in the size of the post-spike afterhyperpolarization (for example, VanDongen et al., 1986; Hounsgaard & Kiehn, 1989).hence steepening the f-I relation of the moto-neuron (for example, Hounsgaard & Kiehn, 1989).Thus, also in this manner synapses can change themotoneuronal responses to driving currents fromelsewhere (for further references concerning theseand other motoneuronal modifications, see Powers& Binder, 2001). Motoneurons innervating differentkinds of muscle units are likely to differ in thecharacteristics of their plateau currents (Lee &Heckman, 1998). To what extent modifications ofexcitability and f-I relation take place incombination with the emergence of plateau currentsis still unclear.

We do not yet understand much about thefunctional role of these various acute changes ofmotoneuronal activation properties. It is essentialto be able to relate these properties to the mannerin which motoneurones are used in motor

behavior. Such problems are presently beingtackled by several groups of investigators,typically using electromyographic techniques forthe recording of motoneuronal discharges in awakeanimals and humans under different conditions (forexample, rats, Eken, 1998; Gorassini et a|., 1999;human subjects, Kiehn & Eken, 1997; Gorassini et

al., 1998; Collins et al., 2002). The studies made so

far give strong indications that motoneuronalplateau currents play a significant role in animal

and human motor behavior under normalconditions, as well as, perhaps even more so, in


cases of long-term spasticity following damage tothe central nervous system (Bennett et al., 2001).Possibly, plateau currents might contribute to thespontaneous motoneuronal activity often seen inpatients after spinal cord injury (Zijdewind &Thomas, 2001).

In addition to the possible long-term effects onplateau-behavior in spasticity, various other kindsof chronic modifications of motoneurons areknown, for example, changes in their activationand membrane properties following long-termalterations of motor activity, following changes ofthe innervation target, and so on (for furtherinformation and references, see Mendell et al., 1994;Munson et al., 1997; Wolpaw & Tennissen, 2001;Beaumont & Gardiner, 2002). Very little is knownabout the mechanisms and precise conditionsunderlying such long-term alterations; this field isimportant for further investigations.

CONCLUDING REMARKS:PROBLEMS AT THE OUTPUT?

In all motor behavior, the properties of thefinal common path of the motor system are

important for defining how it should be run byneuron populations further upstream within thecentral nervous system. As I mentioned at theonset of this brief survey, a non-optimal functionof such ’higher’ mechanisms is probably responsiblefor most motor problems encountered by clumsychildren. Are there any possibilities that the outputsystem might, in itself, also be directly concernedin the production of ’clumsiness’?

I do not, of course, know the answer to thisquestion. Nevertheless, I would like to mention atleast one hypothetical risk factor for furtherconsideration. The short-term modifications of howmotoneurons respond to synaptic activationforexample, as influenced by monoaminergic or othermetabotropic synapsesmight, if badly integrated

into the total motor program, conceivably lead to

unpredictable variations in the forces produced bysets of activated muscles, thereby contributing to a

production of ’clumsiness’. Whether such (or other)problems at the output actually exist in clumsychildren is a question for further experimentalresearch.

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Principles of Force Gradation in Skeletal Musclesdownloads.hindawi.com/journals/np/2003/858709.pdf · muscle force during motor behavior. Basic properties of motoneurons and muscle