RECRUITMENT OF MOTOR UNITS DURING LENGTHENING

CONTRACTIONS OF HUMAN FLEXOR CARPI RADIALIS

Paula J. Foht

BSc, University of Alberta, 1996

BKin, University of Calgary, 1998

THESIS SUBMïiTED IN PARTIAL FüLFiLLMENT OF

THE REQUIREMENTS FOR THE DEGREE OF

MASTER OF SCIENCE

(Neuroph ysiolog y)

in the School of Kinesiology

O Paula J. Foht. 1999

SiMON FRASER UNNERSlTY

December, 1999

Al1 tights feserved. This work may not be

teproduced in whoIe or in part, by photocopy

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The orderly recruitment of motor units according to the size principle has been

show to apply to many different physiological conditions during muscle contractions.

However, exceptions to an orderly recmitment of motor units have been claimed during

muscle lengthening (eccentric) contractions by Nardone et al. (1989) and Howell et ai.

(1995) and have gained acceptance in the literature (Binder et al., 1996). According to these

authors, lengthening contractions involve a selective recruitment of large, fast-twitch motor

units with derecruitment of smail slow-twitch motot units. Careful examination of their data,

leads to questions about their interpretation. Therefore, the goal of this project was to study

the recmitment order of motor units in flexor carpi radialis during lengthening contraction of

wrist flexors. The subject contracted the wrist flexors isometrically against a background

load and recruited at least one discemible active motor unit. A lengthening contraction

followed this isometric phase. In the first paradigm a lengthening contraction was produced

when the subject yielded CO a constant Ioad and allowed the wrist to be extended. The second

paradigrn involved an additional ramp increase in load superimposed on the isometric

contraction producing a lengthening contraction or a step increase in load applied to the wrist

producing a very fast lengthening contraction resuiting in a stretch reflex. The results

showed a variety of motor unit recruitment and firing patterns during the lengthening phases

of contraction. However, no systematic selective recniiûnent was observed. The tonic lower

threshold motor units either changed their firing rate or were derecmited. If an additional

motor unit(s) was recruited during the lengthening contraction, it was the next higher

threshold unit and not a selectively activated large, high threshold unit. Our study further

supports the universality of the size principle of motor unit reccuitment.

DEDICATION

To my parents who give me al1 the encouragement, support and love a daughter needs.

1 would like to thank Dr. Parveen Bawa, first of al1 for the incredible

opponunity to do this research, as well as for her continuous patience and support dong the

way. I would also like to thank Dr. John Dickinson, Dr. Wade Parkhouse and Dr. Charles

Krieger for their assistance on this thesis. Thanks to my family for always king just a phone

cal1 away when 1 needed them. Finally, 1 would like to thank James, but words cannot

express how much 1 cherish him for his encouraging inspiration, unselfish support and most

of al1 for his endless love during this graduate degree.

Angular Displacement and Velocity ............................................................. 36

Angular Displacements and Mean Angular Velocities ........................................... 40 Constant Load hngthening Contractions .............................................................. 45

............................................................................................................ Preloads 45 . . Tension and Position ........................................................................................ 46 Single Motor Unit Responses .................................................................... .A6 Surface EMG ................................................................................................... 52 Unusual Recruitment and Firing of Single Motor Units ................................. 54 Cornparison of two types of Lengthening Contractions .................................. 55 Oscillatory Behaviour ...................................................................................... 56

Im@ Ramp Load Lengthening Contractions .................................................... 56 Preloads and Imposed Ramp Loads ................ .. ............... .. .... -56 . . Tension and Position ........................................................................................ 56 Single Motor Unit Responses ......................................................................... -57

................................................................................................... Surface EMG 62 Unusual RecnWtment and Firing of Single Motor Units ................................. 63

................ ..................*........................................*.... OsciHatory Behaviour .. 66

Im@ Step L o d Lengthening Contractions ................................................... 66

EMG Tremor ............................................................................................................. 68

............................................................. Summary d Motor Unit Firing Behaviour 68

............................................................................... Limitations OP the Sîudy. 1

Angular Displacement and Velocity ......................................................................... 73 Single Motor Unit Recruitment and Firing Pattern .............................................. 75

Comparison of the Two Types of Constant Load Lengthening Contractions .. 75 ................................................................................................. Constant Lods 76

Tmposed Ramp Loads ..................................................... .. 77 ............................ ....................................................................................... Imposed Step Loads -78

Surface EMG .............................................................................................................. 78

Input to the Motor Uniîs ........................................................................................... 82 .................................................................................................................. Conclusion 83

vii

LIST OF TABLES AND FIGURES

Table 1: Summary of the parameten generated for each motor unit and each individual ............................................................................................. leagthening contraction 34

............................... Table 2: Mean surface EMG for constant load lengthening contractions 53

Table 3: Mean surface EMG for imposed load lengthening contractions ............................... 62

................................................................................ Figure 1: Apparatus set-up 23

.............. Figure 2: Front view of gravitational load attached to the handle of the apparatus 24

....... Figure 3(A-C): Set-up for experimental recording of SMU. flexor and extensor EMG 25

Figure 3(D-G): Set-up for experimental recording of position. tension. toque load. preload. ....................................................................................... and trigger 27

Figure 4: (A) Experimentai set-up used to produce the position template (B) Example of ................................ position template of camp profile that subjects followed 29

Figure 5: Experimental set-up for generation of step and rarnp increase imposed load ................................. lengthening contractions produced by the torque motor 30

Figure 6: Set-up for data ................................................................................. 33

Figure 7: Drawing of exarnples of constant and imposed load lengthening contractions .......................................................... preceded by isometric contraction 37

Figure 8: Frequency distribution of angular displacement during constant load lengthening ..................................................................................... contractions 41

Figure 9: Frequency distribution of angular displacement during imposed load lengthening ...................................................................................... contractions 41

Figure 10: Frequency distribution of mean angular velocity during constant load lengthening .................................................................................... contractions 43

Figure 1 1: Frequency distribution of mean angular velocity during imposed load lengthening .................................................................................... contractions 43

.................................. Figure 12: Frequency distribution of total angular displacement 44

......................................... Figure 13: Frequency distribution of totai angular velocity 45

Figure 14: Tension and position traces of constant gravitational load lengthening contraction ......... iiîustrating biphasic pattern of tension during fast lengthening contractions 47

Figure 15: Typical resdts from constant load lengthening contractions paradigm showing ........................................................ silencing of tonic single motor units 48

Figure 16: Typicai results h m constant load lengthening contractions paradigm showing .................................................. continuation of single motor unit activity 50

Figure 17: Typicai results h m constant load lengthening contractions paradigm showing re- ..................................................... recruitment of tonic single motor units 51

........... Figure 18: Typical example of EMG during constant load lengthening contraction 54

Figure 19: Example of unusual pattern of recruitment during constant load lengthening ..................................................................................... contractions 55

......... Figure 20: Tension and position traces during imposed load lengthening contraction 57

Figure 21: Typicai results from imposed load lengthening contractions paradigm showing ................................................................ silencing of tonic motor units 59

Figure 22: Typicai results from imposed load lengthening contractions paradigm showing .................................................. continuation of single motor unit activity 60

Figure 23: Typicai results from imposed load lengthening contractions paradigm showing continuation of single motor unit activity over two different speeds ................... 61

Figure 2 4 Typical resuits h m imposed load lengthening contractions paradigrn showing ................................................ rec~itment of additional single motor units 62

........... Figure 25: Typicai exarnple of EMG during imposed load lengthening contractions 65

Figure 26: Example of recruitment of larger threshold unit during imposed load lengthening ....................................................................................... contraction 65

..... Figure 27: Typicai resuiis from step torque pulse imposed load Iengîhening contraction 67

..................... Figure 28: Example of accentuated tremor during lengthening contractions 69

..................... Figure 29: ExampIe of tremor during imposed load lengthening contraction 70

INTRODUCTION

Neucomusdar Control

Motor commands fiom the centrat nervous system are expressed through

changes in the magnitude of neural excitation of skeletal muscle. These changes in muscle

excitation generate force and movement, the magnitude and direction of which depends on

the properties of the muscle tissue and the mechanical loads experienced by the muscle.

Force control in a skeletal muscle is governed ùoeh by descending and reflex inputs

converging on motoneurons. Motoneurons integrate dl inputs (excitatory and inhibitory)

and, in turn, excite the muscle.

The totd force output of a siceletal muscle can be graded in two ways. First,

different numbers of motor units cari be remit& or derecniited. The second mode of force

regdation is achieved by changing the rate of discharge of individual motoneurons by rate

coding. Rate coding alter5 the force output of individual single motor units by using their

capacity to produce a partially fus& tetanus, in which the mean force output becomes

progressiveIy greater with increasing rate of motoneuron discharge. The total force of an

individual motor unit depends on the size of the motor unit and the rate of discharge. In

general, the relative contributions of rate coding and recruitment to muscle force output vary

widely from one muscle to another and depend on tbe types of motor units comprising the

muscle (Freund, 1983).

Mutor Unit a d the Motoneuron P d

A motor unit includes an alpha motoneuron and al1 ihe muscle fibres

innervatsd by it. M e n an alpha motoneuron discharges under normal circumstances, al1

muscie fibres of the motor unit contract, and a particular alpha motoneuron may participate in

a variety of reflexive and voluntary movements. Synaptic input h m a variety of sources

converge on the a-motoneuron where it semes as the last stage of integration to shape a

motor output to the muscle.

A given skeletal muscle is innervated by a set of alpha motoneurons that

comprise the motoneuron pool of the muscle. In the spinal cord, the somata of the

motoneurons constituting a motoneuron pool are arranged in longitudinai columns extending

rostrocaudally in Rexed's lamina IX of the ventral hom of the grey matter. The location of

different motoneuron pools is somatotopicaily relateci to that of their muscles, and

motoneuron pooh that innervate axial musculature tend to be located mediaily while those

innervating limb musculature are located laterdly (Brown, 198 1).

Alpha motoneurons of a pool Vary in size, biophysical properties including

input resistance, axon diameter, conduction velacity, and depth and duration of after-

hyperpolarization (Burke, 198 1; Henneman and Mendell, 1981). The relationship between

electrophysiological propetties of rnotoneurons and contractile responses of the muscle

fibres, which has k e n reported in several muscles throughout the body for hurnans and other

species, is described below and has implications for tecniitment patterns of motor units

(Burke, 198 1; He~eman and Mencieu, 1981). Srnalier, slower conducting motoneurons with

low rheobase values generaily innervate type 1 (SOG) muscle fibres. (The rheobase value is

the minimum current input to the motoneUron needed to elicit an action potential.) These

muscle fibres produce s m d tetanic forces and are fatigue cesistant. Small motonemns have

longer afterhyperpolarization which Limit these motonemns to fm at lower rates. These

motor uni& with long contraction times need very low rates to fuse, hence they are innervated

by motoneurons with longer afterhyperpolarizations. Medium diameter motonewons

innervate type IIA (Fûû) muscle fibres, which have medium to large tetanic force. Larger,

fast conducting motoneurons with high rheobase values tend to innervate type IIB (FG),

which produce very large tetanic force. Fast contracting motor units require higher firing

rates for fusion and are appropriately innervated by motoneurons with short duration

afterhypolarizations. The electrophysiologicai characteristics of the motoneurons that supply

slow and fast twitch muscle fibres differ and are, in part, responsible for the specific firing

patterns of these cells.

In order to classify motor units, Burke et ai. (1973) used the technique

introduced by Edstfim and Kugelberg (1969). The latter authors showed that by electrically

stimulating single motoneurons, it is possible to elicit tetanic contractions of muscle fibres

belonging to the same motor units. Prolonged tetanic activity of muscle fibres of a motor unit

depletes it of glycogen. Such fibres are distinguished from the rest of the muscle fibres by

the absence of glycogen in stained cross-sections of the muscle. Initidy, Burke (1967)

divided motor units into two groups: type S motor units are those that contain slow type 1

(SO) muscle fibres and type F motor units are those that contain fast contracting motor units

having type iI muscle fibres. Subsequently, the fast contracting motor units were

subdivided into two categones on the basis of theh susceptibility to fatigue: fast fatigue

resistant (FR) and fast fatiguable (FF) motor units, whose muscle fibres were found to be type

IIa (FOG) and type IIb (FG), respectively (Burke et ai., 1973).

The physiological and biochemical properties of motor can be divided

into distinct types, and the differentiation of motor units into types is helpfd in understanding

the neural control of motor units. However, in reality, motor unit properties show a

continuous variation in properties such as maximal tetanic force, isometric twitch contraction

time and amplitude, and fatigue tesistance (Freund, 1983), and a continuous spectrum of a-

motoneurons properties ranging from S to FF type characteristics exists (Henneman, et al.,

i974). The studies involving cat motor units and other animal models have provideci

fundamental information in regard to motor units. Using the pnnciples that are well

established in the cat motor units, information can be extrapolated to human rnotor units. Al1

properties do not transfer directly, but ovedl, it is fair to conclude that the organization of

motor unit populations in humans is basically the same as found in rnany mammalian

muscles (Burke, 198 1).

Muscle Activation

The central nervous system controls and monitors movement by transmitting

to and receiving signals h m muscle through an extensive neural network. Every cell of a

motoneuron pool is activated through a large number of spinal and supraspinal neural inputs.

Spinal inputs affecting motoneurons originate fiom muscle spindles, golgi tendon organs,

joint and cutaneous receptors, and spinal intemeurons while supraspinal pathways that input

ont0 the motoneurons include the corticospinal tract originating h m the cerebrai cortex, the

rubrospinal tract originating h m the red nucleus, the vesti%ulospinal tract originating h m

the vestibular nuclei and the reticuiospinal tract originating fiom the reticuiar formation.

Patterns of single motor unit activity in animals and humaas have provided

insight into the neuromuscular control of muscle. One such study led to the 'size principle*

of motor unit tecruitment which enunciated that to achieve a smooth graduai increase in

force, smail motor units that are normally composed of slow twitch fatigue cesistant fibres,

are recruited before large motor units that are usually composed of fast twitch, fatiguable

muscle fibres. Because most muscles are composed of motor units of heterogeneous

properties, the precise order of motor unit recmitment will greatly affect the output.

Recruitment of Motor Units

ûrderly Recruitment according to the Size tinciple

The 'size principle' proposed by Henneman and his CO-workers (Henneman,

1957; Henneman and Olson, 1965; Henneman et al., 1965, 1974) is the orderly recruitment of

motor units according to their size, i.e. small motor units have lower thresholds than, and are

thus recruited before, large motor units. Using recordings obtained h m smali numbers of

motor axons in fine filaments of ventral mot of decerebrate cats, the authors found that

motoneurons with srnail amplitude axonal action potentials were recmited fmt in response to

muscle süetch (Henneman et al., 1965). Muscle stretch increases excitatory spindle afferent

input to motoneurons. As the amount of stretch was increased, these small motoneumns

increased their firing rate as other motoneurons with larger amplitude action potentiais were

recniited. When the amount of stretch was decreased, motor axons showing the lowest-

amplitude action potentials wece the last to be derecruited.

Recruitment was found to be ordered according to the amplitude of the motor

axon action potential where motoneurons with smali action potentials were recniited before

motoneurons with large amplitudes. Since the amplitude of recorded axonal action potential

is directly related to the diameter of its axon, it can be postulateci that motoneurons are

recniited in order of increasing axonal diameter (Clamann and Henneman, 1976). Further,

axonai diameter is proportional to the toiai surface area of the motoneuron (Clamann and

Henneman, 1976), so it follows that motoneurons are recruited by excitatory inputs in order

of increasing size of the motoneunin. As weU, the axon diameter that varies with

motoneuron size, influences the velocity at which action potentials are propagated. Thus,

rnotor axonal conduction velocity was also found to be related to motoneuron size

(Henneman and Mendell, 1981; Bawa et al., 1984).

Additional studies revealed that such recruitment could be observed under a

variety of different activation conditions (Henneman et al., 1965). Excitatory and inhibitory

inputs to motoneurons from the peripheral and supraspinal systems were produced to test the

recruitment pattern of motor units. For a net excitatory input to a motoneuron pool, a

characteristic order of recniitment was always obsewed, and for an overall inhibitory input, a

systernatic deremitment of motor units was observed (Henneman and Mendeil, 198 1). The

size of the motoneuron, and thus the motor unit, is important in detennining its response to

synaptic influences. "As a result of many of the inherent properties of motoneurons, and

various inputs to the pools, orderly rec~iîment of motoneurons of skeletal muscles is very

robust" (Binder et ai., 1996).

Motor Unit Recruümeni in Humans

Human studies do not permit investigations into the synaptic and cellular

mechanisms of the size principle, but they allow one to approach the matter h m a functional

6

viewpoint. In this case, one monitors whether motor unit behaviow follows this principle

duriag natural muscle contraction under different voluntary conditions for different motor

tasks. Numerous experiments have been conducted on animal and human muscles, during

both voluntary and reflex contractions, to ascertain whether the size principle of orderly

recniitment applies. It has been shown to prevail with only a few possible physiologically

relevant exceptions reported to date (See Reviews: Henneman and Mendell, 198 1; Calancie

and Bawa, 1990; Cope and Clark, 1995; Binder et al., 1996).

Isometric voluntary contractions

The orderly pattern of recniitrnent was first shown to apply to humans during

isometric voluntary contractions of first dorsal interosseous muscle by Milner-Brown et al.

(1973b). The contractile twitch force generated by individual motor units was computed by

recording the motor unit potential with a selective needle electrode inserted into the first

dorsal interosseous muscle and recording the tension produced by the muscle. Spike

tciggered averaging was used to extract the twitch force that was correlatexi with each

discharge of the single motor unit. A nearly linear relationship was obsewed between the

twitch tension generated by the rnotor unit and threshold voluntary force level at which the

motor unit became active. This force thteshold is d i i t l y proportional to the total input to

the motoneuron pooi which in turn, is related to the net synaptic input arriving at each

motoneuron.

Similar recmitment patterns have been shown during slow voluntacy isometric

contractions of many human muscles including the extensor digitonun cornmunis (Mooster

and Chan, 1977; Riek and Bawa, 1992), the masseter and the temporaki (Yemm, 1977), the

flexor carpi radialis (Calancie and Bawa, 198!%), the flexor carpi ulnaris (Jones et al., 1993),

the abductor pollicis brevis (Thomas et al., 1987), and the extensor carpi radialis (Riek and

Bawa, 1992).

Direction-dependent motor unit recniiûmnt patterns have been reported when

a muscle is perforrning different voluntary tasks. Muscles including the first dorsal

interosseous (Desmedt and Godaux, 198 i; Thomas et al., 1987), the abductor pollicis brevis

(Thomas et al., 1987). and the biceps brachii (Ter Haar Romeny et al., 1984) have shown the

task group pattern of motor unit recruitment. These studies suggests that motor units tended

to be preferentially recmited for one task over another task. However, muscles with

identified task groups in which al1 the motor units contribute to a specific contraction, are not

exceptions to an orderly rec~itment of motor units. Using the extensor digitomm conununis,

recniitment of motor units within each individual task group was found to be according to the

size principle (Riek and Bawa, 1992). Extensions of the middle and ring finger were

periormed separately and together, as welj as extension of the wrist, and for each subgroup or

task group of the EDC motoneuron pool, motor unit recruitment thresholds were plotted

against their twitch tension and as with other isometric motor unit recruitment studies, an

orderly recruitment was seen for each task group (Riek and Bawa, 1992). A muscle once

thought to possess task groups, the flexor carpi ulnaris muscle was studied during isometric

flexion and ulnar deviation, CO-contraction of wrist flexors and extensors and non-isometric

flexion of the wrist (Jones et al., 1993). No task group was observed in FCU, all motor uaits

contributed to each of the four tasks, and orderly reccuitment was observecl in each of the four

tasks.

Grimby and Hannerz (1968) studied the recruitment order of motor units on

voluntary contraction of human tibia1 muscle using needle electrodes. They claimed that the

recruitment order of motor units is different in tonic and phasic activity. A rapid contraction

was said to be initiated by large unit and then sustained by a smdler unit that sustained

isometric contraction, They conc~udtxî that a human could selectively activate appropriate

motor units depending on the task (Grimby and Hannen, 1973). Desmedt and Godaux

(1977) did not find such selective recruitment during a more thorough investigation of tonic

and phasic voluntary activity. These authors studied pairs of motor units of the tibialis

anterior during fast baiiistic contractions as well as slow ramp contractions. The recruitment

threshold of motor units during ballistic contractions was show to be dependent on the rate

of change in muscle force. This phenomenon of high rates of change in force decreasing the

recmitment threshold for the motor units has been well documented (Tanji and Kato, 1973;

Desmedt and Godaux, 1977; 198 1). Due to difficulties in establishing a recruitment

threshold of units during ballistic contractions, the ballistic threshold of motor unit was

determined to be the mean force at which the motor unit always fired. The rank order of

pairs of motor units was established with this method and motor units were found to follow

an orderly recmitment. Reversais of recruitment were seen in about 11% of the trials, but

largely between units with similar recmitment thresholds.

Reflexve contractions

During slow voluntary activation, motor units are recruited and discharge

tonicaiiy. During reflexes produced by aimost syncbnous affecent inputs, a motor unit

responds phasicaliy, wirh genedy only one spike in response to the input. The single motor

unit activity during fast stretch reflexes imposed by toque motors was examined and the

orderly recruitment of motor units was obse~ed during the süetch reflexes in humans

(Calancie and Bawa, 1985a). Through observance of the surface EMG in the upper limb

muscles, a sudden stretch to a muscle results in two distinct periods of muscle activity: a

short latency response occumng approximately 25 to 50 rns after onset of stretch and a long

latency response occumng approximately 50 to 90 ms &et the onset of the stretch (Calancie

and Bawa, 1985a). The short latency response is thought to be mediated by the muscle

spindles via the spinal stretch reflex pathway wMe the long latency response is thought to be

mediated through suprapinal pathways. Both responses precede the voluntary response that

occurs after approximately 100 ms. Due to ihe probabilistic nature of motoneuron response

to phasic input, reflex responses are averaged over a large number of inputs. The magnitude

of the response is measured in terms of the number of discharges per input, which represents

the response probability (Calancie and Bawa, 1985a). It was shown that a motor unit's

response probability during both the short and long latency reflex periods was higher for the

lower threshold units than for motor units of higher recruitment thresholds. This suggested

that descending motor pathways and afferent fibres have a similar organization in terms of

inputs to the motoneuron pool. The probability of response was found to be dependent on

many properties including the level of facilitation of the motoneunin pool (background

activity), the strength of the imposed perturbation, and the preparatory set of the subject, yet

the recniitment order remaineci unchanged (Calancie and Bawa, 1985a).

Voluntary dynamic contractions

Voluntaq dynamic contractions incIude shortenhg (concentric) contractions

during which an active muscle shortens during movement and lengthening (eccentric)

10

contractions during which an active muscle is lengthened dwing movement. In comparison

to isometric contractions, there are relatively fewer studies of the motor unit rec~itment and

firing pattern during dynamic contractions. During dynamic contractions, variation in the

shape and amplitude of the motor unit action potential due to the relative movement of the

intramuscular electroâe with respect to the motor units that are recorded can increase the

difficulty in motor unit identification. It can also be difficult to ascertain whether the

observance of the onset of an action potential is a result of recmitment of a new unit or due to

delayed recording of an already active unit because of movement of the electrode during the

change in muscle length.

The orderly recruitment of motor units according to the size principle has ken

shown to occur during human voluntary dynamic movements. Thomas et al. (1987) observed

28 motor unit pairs from the first dorsal interosseous and 9 motor unit pairs from the

abductor pollicis brevis during a repetitive opening and closing of scissors movement. The

relative rank order recruitment thresholds for pairs of motor units observed during the

dynamic movements was determined through cemitment during voluntary isometric

contraction of the units. Motor uni& had recruitment thresholds up to approximately 50%

maximum voluntary contraction. Motor unit recruitment order, according to increasing

twitch tension amplitude, was preserved during repetitive dynarnic movements. Four pairs of

rnotor units (14%) from first dorsal interosseous and two pairs (22%) from abductor pollicis

brevis, showed recruiîment reversais for more than 50% of scissor movements. However,

these unit pairs showed similar recruitment thresholds. Therefore, motor unit recniitment

was predominantly ordered by size during repetitive scissor movements, with signincant

number of reversais for units of simiiar thresholds.

in addition to firing of motor units of similar thresholds, hi& rate of reversals

have been attributed to the pbasic nature of contractions l i e the scissor movement performed

in the study by Thomas et ai. (1987). Phasic contractions that involve a fast and large input

to the motor unit and result in a brief discharge of a small number of action potentiais can

lead to revenais because of the prababilistic nature of response, In a later study using the

fmt dorsal intemsseous muscle during tonic functional tasks, Jones et ai. (1994) observed

less than 10% of recruitment reversals. An orderly recruitment of motor units was show to

occur during these tonic contractions involving abduction of the index finger, rotation of a

knob and pincer grip of a clip. Tonic contractions where the increasing torque over the

different functional task contractions was canied out over relatively longer periods showed

significantly less reversals. When an input to the motoneuron is phasic, reversals have a

higher probability of occurring due to noisy input to the motoneuron. Because of this noise,

reversals are more likely between motoneurons of similar threshold, and less probable

between units with a large difference in thresholds. A third factor which can contribute to

reversals between motor units of different sizes is the axonai conduction velocity. Desmedt

and Godaux (1977) attributed the reversals they found during ballistic contractions to

differences in conduction velocities of units with similar recniitment thresholds.

Using intrmuscular EMG recordings of the biceps brachii, Moritani et al.

(1988) observed the activity of motor units during shortenhg and lengthening contractions.

Both types of contractions involved 120 degrees of movement, h m 30 and 150 degrees for

shortenhg and lengthening contractions, respectively, with full extension at O degrees in 5

seconds agaiast a 3û% maximum voluntary contraction quivalent load, Greater

motor unit activity (as estimated h m population EMG) and the presence of motor units with

12

relatively large spike amplitudes were seen during shortening contractions in comparison to

lengthening contractions at three separate positions (45,90, 135 degrees). The data showed

that lengthening contractions were associated with less motor unit activity as demonstrated by

recniitment of relatively smail spike amplitude motor units and less marked rate modulation

compareci to shortening contractions. Smaller spike amplitudes and lower spike frequencies

were seen at ail three angles, although only 2 out of 3 joint angles of each property were

significant. The recruitment pattern of the motor units indicated that different threshold

motor units were usually recmited in order of increasing spike amplitude even at higher

levels of muscle contractions.

Sogaard et al. (1996) and Kossev and Christova (1998) studied specifically the

motor unit recmitment patterns of the biceps brachii during shortening and lengthening

dynamic contractions. Sogaard et al, (1996) used loads of approximately 10% MVC. A total

of 1 19 motor units were identified during dynamic contractions at mean angular velocities of

10 degrees per second and were examined for recruitment pattern. Several contractions of 20

degrees per second and 40 degrees per second were perfonned with 30 and 9 identified motor

units, respectively. ûver 60% of the identified motor units were found to be active in both

shortening and lengthening contractions for each velocity. Further, no significant difference

in amplitude, duration or area of the motor units were found between the set of motor units

that were active only during the shortening phase, lengthening phase or both phases. The rate

modulation was deemed the important difference between shortening and lengihening

contractions and not the selective m i t m e n t of motor units during each typ of contraction.

Mean fiting rate of the motor units decreased ~ign~cantly when the contraction changed

h m a shortening to a lengthening contraction, and this lower mean firing rate during

13

lengthening contractions has also been found in other studies on decerebrate cats (Cordo and

Rymer, 1982) and in humans (Tax et al., 1990).

Using the biceps brachii muscle, Kossev and Christova (1998) identified 45

motor units during shortening and lengthening contractions. The subjects performed

contractions of slow (4.94 I 5.3 Nmis) and fast (9.20 110.05 Nmls) velocities with a mean of

24.96 14.30 % maximum voluntary contraction and a high limit of 52 % MVC for the

relative workloads. Al1 but one of the motor units that they investigated were active during

both the shortening and lengtbening contraction phases as weil as during isometric

contractions. The one motor unit that was active only during the shortening and isometric

contractions was derecruited pcior to the lengthening contraction. An orderly recruitment and

detecruitment of motor units with respect to their isometric remitment threshold was seen

although they observed thai the recruitment threshold during the shortening phase was found

to be lower than the detecruitment threshold during the lengthening phase of particular motor

units. Generally, the derecruitment of motor units during a lengthening contraction was the

reverse of the recruitment during the shortening.

AUernative Patterns of Motor Unit Recruitnient

While some reversais in recruitment order are seen in nearly al1 experirnents

focused on the recmitment of motor units, orderfy recruitment of motor units has been

generally observed (Henneman and Mendell, 1981; Cope and Clark, 1995) in a variety of

different studies. However, some sudies suggest deviations k m the size-ordered

remitment under specific conditions. These studies include electricd stimulation of

cutaneous afferents (Kanda et ai., 1977; Garnett and Stepheas, 1980,198 1; Masakado et ai.,

14

L991) and of muscle afferents (Davies et ai., 1993). As well, a few studies have claimed

lengthening contractions as possible exceptions to the orderly recruitment of motor units

(Nardone et ai., 1989; Howell et al., 1995).

Studies using cutaneous input to the motoneuron have proposed exceptions to

the size principle. in decerebrate cab, it was shown that cutaneous input from the sural nerve

superimposed on stretch reflexes or tendon vibration refiexes tended to decrease the firing

rate of relatively low threshold medial gasûacnemius motoneurons while increasing the

excitation of the higher threshold motoneurons (Kanda et al., 1977). The larger motoneurons

were said to receive a pa ter amount of excitatory input while the smaller motoneurons

received a proportionally greater amount of inhibition. With this activation pattern, large

motoneurons would be recniited in preference to the small motoneurons, and such a

recruitment scheme could be considered an exception to the size principle.

Clark et ai. (1993) attempted to conficm the findings under similar conditions

in the decerebrate cat. The study found a smdl percentage of medial gastrocnemius motor

units with slow axonal conduction velocity exhibited a slowing of their firing rates during

cutaneous input produced by skin pinch. However, when pairs of motor units were recniited

purely by tendon vibration, or skin pinch or elacîrical stimulation of the sural nerve,

recruitment order was the same and the lower tbreshold unit had the slower conduction

velocity in 90% of cases. Thus the size principle recmitment scheme was used during both

peripheral Ia and cutaneous input to the medial gastrocnemius motoneuron pool.

In humans, cutaneous stimulation has also been used to demonstrate the

possibility of exceptions to the size principle (Stephens et al., 1978; Gamett and Stephens,

1980,1981). in this case electncai stimulation of the digital nerves of the index figer

15

demonsûated tendencies toward inhibition of f ~ n g of lower threshold units and facilitation

in higher threshold units. The physiological relevance of electrical stimulation bas been

questioned because normal tactile stimulation of the index finger did not produce disorderly

m i n n e n t of motor units (Cope and Clark, 1995). Fwthermore, since this change was

observed after 5 minutes of continuous firing of motor unit, the question of fatigue may

complicate the explanation of observed pattern.

Lengthening Conîmcîions as Possible Excepiions to Orderly Recruitment

Contrary to the comprehensive evidence suggesting that motor unit

recruitment occurs according to the size principle, possible exceptions have been reported.

As previously mentioned, some investigators have implicated lengthening contractions to

involve an alternative recruitment pattern of motor units where large fast-twitch motor units

are recruited selectively instead of small slow-twitch motor units.

In 1989, Nardone et al. recorded the single motor unit activity of the soleus, medial

and lateral gastrocnemii muscles, as well as the position signal during isotonic contractions.

Using 15-20% maximum voluntary contraction loads, the subject either maintained an

isometric contraction, performed a shortening contractions in which the ankie was extended

through shortening of ankle extensors, or performed a lengthening contractions in which the

ankle was flexed through lengthening of active ankie extensors. The velocities of the

dynamic contractions ranged h m 10 to 70 degrees per second. Approxirnately 70% of the

identified motor units were reported to be active exclusively in either the shortening or the

lengthening phases. The motor units active exclusively during Iengthening contractions bad a

higher mean isameiric recniitmeat threshold (55.2 I 6.1 Nm) compared to the motor uniîs

16

that were recruited exclusively during shortening contractions (34.8 I22.6 Nm) and the motor

units tbat were active during both the shortening and lengthening phases (27.2 I Nm). The

authors claimed that during the lengthening contractions, high threshold, fast twitch large

motor units were recruited selectively as low threshold, slow twitch small motor units were

preferentially derecmited.

Nardone et al. also reported an increase in EMG activity during the

lengthening contractions. They argued that the larger magnitude of surface EMG during

lengthening contractions was due to recruitment of very large motor uni& wfiich not only

compensated for the derecruitment of small motor units, but resulted in an overail increase in

EMG activity during the lengthening contractions. This was used as additionai support for

their theory of selective recruitment of large units.

The relaxation times of the motor units were presented as a plausible argument

to support the reported selective recruitment of fast motor units over the slow motor units

during rapid lengthening. They hypothesized that lengthening contractions perfonned by the

derecruitment of the fast conducting-fast relaxing large motor units of the agonist muscle

would be more advantageous than the derecruitment of slow conducting-slow relaxing motor

units, since the force developed by the large motor units would terminate faster. They also

suggested that the use of fast-twitch units with their fast relaxation times is necessary for

control of fast lengthening contractions (Nardone et al., 1989). However, tbis rationale seems

questionable for constant load lengthening contractions, for in order to yield to a lad, a

decrease in the force generated by a muscle is required. It would seem inefficient for the

centrai nervous system to first recruit large motor units which generate large amounts of force

when the goai of the muscle is to obtain a decrease in force.

Investigation by Howeii et d.(1995) of the single motor unit activity of the

fmt dorsal interosseous was petformeci during sinusoidal shortening and lengthening

contractions. They reprted selective recniitment chuing lengthening contractions of 3 out of

21 (14%) motor units studied. From this 14 % pattern, they concwred with the hypothesis of

Nardone et al. (1989) that there is a selective reçruitment of motor units during lengthening

contractions. The 3 motor units were said to be recruited when other units were seen to be

decreasing their discharge rate or were king derecniited. However, their results do not

clearly show a pattern of selective recruitment. First, they observed an alternative

recruitment strategy in only 14% of their units and secondly, these units had relatively low

thresholds with respect to the motor unit population. Secondly, their figures illustrate that

two of the three motor units fimd with smaller threshold units fung in the background.

Thecefore, only one of the motor units had an unusual firing pattern. Furthemore, the

lengthening contractions of their subjects were not smooth, but dispiayed imgularities in

their position traces. The position traces showed clear oscillations during the lengthening

contraction, which implied that the lengthening contractions were superimposed by ballistic

shortening contractions. The ballistic contractions of the subjects could have resulted in

bursts of additional higber threshold motor unit activity during the lengthening contraction.

Importance of Lengthening Contractions

iengthening contractions occur when a load is applied to an active muscle,

which is greater than the force generated by the muscle. The source of the load developing

the extemal force could be gravity, the muscle action of an antagonist muscle p u p or an

externaüy applied load. General functions of lengthening contractions include deceleration

18

of body segments, increased mechanical advantage, spring-lie functioas, and shock

absorption. Decelention happens in throwing, where deceleration of the forearm by a

lengthening contraction of the elbow flexors is essential to prevent elbow injury; and durhg

running in which a lengthening contraction of the hamstrings decelerates the swinging leg.

Shock absorption is achieved by the lengthening quadriceps femoris at foot strike during

w u n g and running or when landing from a jump. Spring-like functions include the storage

of elastic energy during the lengthening contraction and subsequently transmitting it to a

shoriening contraction dunng a jump such as when the hamsûings lengthen to lower the thigh

in flexion in preparation to jump and then the hamstrings shorten to raise the thigh in

extension. In conclusion, lengthening contractions are relevant physiologicaliy and hence an

understanding of the types of motor unit firing during this phase is essential.

Objectives of the Thesis

Conflicting evidence exists in studies involving the f i n g pattern of motor

units during lengthening contractions. Some studies have shown an orderly recniitment of

motot units fmm smail to large during lengthening contractions (Thomas et ai, 1987;

Moritani et al., 1988; Sogaard et al., 1996; Kossev and Christova, 1998) while studies by

Nardone et ai. (1989) and Howell et d. (1995) suggest selective recmiûnent of large fast-

twitch motor units accompankd by dececruitment of small slow-twitch motor units. This

'evidence'bas gained acceptance in the litetature (Bin&r et al., 1996). The data in the studies

of Nardone et al. (1989) and Howell et al. (1995) are not convincing as îhere data can be

interpreted differenily.

Therefore, tfie goal of this pmject was to examine motor unit d t m e n t and

firing pattern during lengthening conttactions. A comprehensive investigation involving

lengthening contractions of varying background activity, velocities and loads was perfomed

with the human flexor carpi radialis in order to characterize the motor unit recmitment and

firing pattern during lengthening contractions. Our hypothesis was that motor unit

recruitment during lengthening contractions would follow the six principle of orderly

recmitment. The size pnnciple has been shown in virtually al1 types of muscle contractions

and the evidence for selective recmitment during lengthening contractions is not convincing.

To constitute a systematic pattern by the central nervous system for selective recmitment of

large motor units, clear and consistent evidence would have to be obtained during the

lengthening contractions. This evidence would have to include repeated trials with

unarnbiguous selective mmitment of a high threshold unit(s) with distinct derecmitment of a

low threshold motor unit(s).

Generai Overview

To examine the recruitment of motor units during lengthening contractions,

subjects performed initial isomeûic contractions followed by lengthening contractions of

wrist flexors at various velocities. The first paradigm involved constant load lengthening

contractions either with constant gravitational loads produced by attaching weights or with

constant cunent loads produced by a toque motor. The subject conuacted the wrist flexors

isometrically against a background load then decreased the tension generated by the muscles

so that the constant load extended the wrist joint, thus producing a lengthening contraction of

the active muscles. The second paradigm involved imposed load lengthening contractions

which included camp increases and step increases in load. Again, the subject began by

contracting the wrist flexors isometrically against a background load. An additional ramp

increase in load at various velocities or a step increase in load was applied to the wrist joint

while the subject tried to maintain aconstant contraction in the muscle. The additional load

extended the wrist producing a lengthening contraction.

Subjects

The experiments were conducted on the wrist flexors of six volunteers (2 male

and 4 female). Subjects were right-handed with no history of neurological disease and ranged

in age ftom 22 to 55 years old. The experiments were approved by the Ethics Cornmittee for

Human Experiments at Simon Fraser University, and each subject signed the subject consent

fom.

A ~ p a i 9 -

The subjecîs were seated with their cight foreatm rested on a padded

horizontal plaîform. A vertical handle secured against the metacarpophalangeai joint of the

subject's palm was positioned 8-10 cm away from the rotational axis of the wrist. Secwing

the subject's hand to the handle was done to ensure relaxeci fingers during wrist extension. A

horizontal bar equipped with strain gages connected the handle to a vertical shaft of a

precision torque motor (Aeroflex TQ 82W), and h e axis of wrist rotation was coaxial with

that of the toque motor shaft. To prevent lateral movements of the wrist, two padded clamps

were positioned proKimal to the wrist. Figure 1 illustrates the apparatus from a lateral view.

To achieve a constant gravitational load, weights were attached to the handle by way of a

pulley. Figure 2 illustrates the apparatus from the front with the gravitational load set-up.

Data Recordhg

Single motor unit (SMU) electrical activity was recorded from the flexor carpi

radialis (KR) muscle using bipolac intramuscular microelectrodes. These microelectrodes,

which were consmcted in the laboratory, consisted of two 30-50 pm HML coated stainless

steel wire (California Fine Wire Company) inserted into the shaft of a 25 gauge needle and

held in place with epoxy. The microelectrodes were sterilized with rubbing alcohol and

inserted into the FCR. The SMU activity was preampmed (Grass Pl5 AC) with a gain of

100 and filtered with a band pas of 100 Hz - 10 kHz, then filtered with a AC conditionhg

amplifier (100 Hz high pas). The experimentd set-up for the FCR SMU is shown in Figure

3A. The S M ü activity was monitored on an oscilloscope, and an audio speaker for subject

audio-visual feedback. It was recorded on a video cassette recorder (VCR) tape using a

;train Gauges for Tension

Potentiometer - for Position

FExtensor EMG

Torque Motor

Figure 1: The appam~s set-up for aording the FCR SMU activity, the flexor surface EMG, the extensor surface EMG, the tension, and the position.

e Figure 2: Front view of gravitational load attachcd to the handle of the apparatu during constant load lengthening contractions.

DATA RECORDING

30Hz-3KHz Gain LOO

Conditioning Amplifier

- 1401 Plia Interface

{Computer)

Oscilloicopc

I,

-

30Hz-3 KHz Gain1

1401 Plus tnterface

Orilloscopr?

I ~ H z - ~ O W 100 Hz GPinl

Conditioning Amplifier

Rgure %A-C): Tht set-up for expetimentai recordhg of FCR sin& motor unit, k o r FMG and extensor EMG.

Veiter PCM Record#

Vetia PeM Recorder

Prenmpiitier PIS

I,

Conditionhg Amplifier .

Vetlet P a Recordcr

Vetter mode1 4000A pulse code modulator 0 recorder.

Surface electromyographic (EMG) activity was recorded fmm wrist flexon

and extensors (extensor carpi radialis). The skin was prepared by shaving a patch of skin

over the muscle and cleaning it with alcohol. Two 9 mm disc Ag-AgCI electrodes with

electrode cream (Grass EC2) were then secured approximately 2 cm apart on ttie skin over

the muscle ôelly. The signals were fed to a Grass PL5 AC preamplifier where it was

amplified and band passed filtered at 30 Hz - 3 kHz and recorded on a VCR with Vetter PCM

recorder. It wlis viewed simultaneously on an oscilloscope and on the cornputer screen using

a 1401 PLUS Cambridge Electronic Design (CED) interface. The EMG of the wrist extensors

was monitored to ensure the movement of the wrist was accomplished by only the stretch of

the active wrist flexor muscles, and not by activation of the extensors. Voluntary activation

of the extensors would recipmally inhibit flexors and prevent any new recruitment. Figures

3B and 3C illustrate the experimental set-up for flexor and extensor EMG, respectively. A

ground electrode ;vas secured to the right upper arm of the subject.

The angular displacement of the wrist was transduced by a potentiometer

attached to the shaft of the torque motor. The wrist position signal was sent io an amplifier

and then to the Vetter PCM interface for recording, and to an oscilloscope for viewing online.

Figure 3D illustrates the experimental set-up for position. To provide position feedback for

the subject during lengthening contractions, the wrist position was displayed on an

oscilloscope at a slow sweep speed, and the subject was asked to follow the position trace

template provided on the oscilloscope. Three different position templates were coostructed

using a fiitered square pulse generated by a Grass Sa8 stimulator to produce slow, medium

DATA RECORDING (conti)

E Tension

Orillorope for Subject Position

Potentiometer

,

Vetter PCM Recorder

Oscilloscope P--'

DC

Conditioning Ampüfur

I )

- 1401 Interface

amputer

Vetter PCM Recorder

1401 Interface amputer

Bridgc Amplifier

Fi* WG): The sa-up for recordhg of position, teasion, torque bad p W and uigger.

Dc

Vetter PCM Recordrr

ûasr 918 Simulntor

Gnrr 918 3irnuintor

- II)

Conditionhg , Amplifut

Couditionhg - Vettet PCM A m p ü f i kcordcr

Conditioning A m p l f ~ r

DC

v

ami fast velocities. Subjects were not required to trace the template exactly, but were asked

to use it as a guide to produce lengthening contractions of different velocities. The

experimental set-up and an example for the position trace template are shown in figure 4.

To mesure tension produced by the wrist flexors, strain gauges (EA-13-

250MQ-350) were mounted on the horizontal bar connecting the handle to the toque motor.

The tension signal from strain gauges was fed to a bridge amplifier (Vishay Instrument, DC - 1000 Hz band pass) then displayed on an oscilloscope and recorded on a VCR (Vetter PCM

recorder). Figure 3E illustrates the experimental set-up for tension.

The precision torque motor driven by a servo-amplifier was used to provide

resistance to wrist flexion through a background load (preload) during the isomeüic

contractions preceding the constant current load and imposed load lengthening contractions.

The prebad produced by the torque motor was used to control the strength of contraction of

the FCR by activating one or several tonic firing of motor units. Figure 3F illustrates the

experimental set-up for producing torque load. The torque motor also provided the ramp and

step increase in load for the imposed load lengthening contractions and step pulse imposed

load lengthening contractions, respectively. The ramp and step increases in load were

achieved through a triggered square pulse generated by a Grass S88 stimulator that drove the

servo-amplifier of the torque motor. The square pulse was sent directly to the setvo-ampiüïer

for the step load and was low pass filtered at different ftequencies to obtain different rates of

ramp increases in toque load. The details of the experimental set-up for producing ramp and

step increase in loads are show in figure 5. A trigger generated by the Grass S88 stimulator

was used to initiate the ramp and step increase in load of the imposed load lengthening, to

Velociîy

Slow

Medium

Fast

Square Puise

Low uass

0.7 Hz

1.1 Hz

3.0 Hz

Figure 4: (A) The experimental set-up used to m u c e Ihe position template. (B) An example of a position kmplate of a ramp profite that subjects followed voluntarily during constant load lengthening conaactions. The solid line reprcsents the continuous position template that the subjects followed and the dotted line npresents the subject's position signal. The oscilloscope divisions were 200ms horizontally and 05 volts vertically.

,, Filter Position Trace Profle on Oscilloscope

S tep Servo- Torque Amplifier Motor

Trigger Square + Puise

Filters Servo- Torque -b Amplifiei Motor

Duration b w pass Rame Velociiy

1000 ms 0.64.7 Hz Slow

I 800 ms 3 H z Medium

I 700 ms > 10Hz Fast L

Fipn 5: The experimenial set-up for hc generation of step and ramp increase imposed load lengthening contractions produced by the torque motor. As the subject maintain a constant activity in the muscle, the applied load was increased to produce a lengthening contraction.

trigger the computer and as the extemal trigger on the oscilloscope. Figure 3G illustrates the

expecimental set-up generating the trigger.

Experimental Procedure

Subjects were given several practice trials for tracing the given position

templates until a sufficient proficiency was obtained. With a constant preload of either

gravitational or torque motor origin, and siarting h m a position of 10" to 15' of wtist

flexion, the subject was asked to slowIy contract the wrist flexor muscles until a clear tonic

motor unit was recruited. Tonic firing was &fined as a repetitive rhythmic discharge of a

rnotor unit, Several lengthening contractions with the motor unit were perfonned at different

velocities. Then, if possible, an additional motor unit was recruited and the procedures were

30

repeated. The strength of the preload and of the ramp loads was adjusted for clacity in the

motor unit responses. Frequent rest periods were given to the subject to reduce the

probability of fatigue.

The details of experimental pmdigms performed with audio-visual feedback

of the FCR SMU activity and visual feedback of position are:

1. Constant load lengthening contractions. The subject was asked to hold an

isometric contraction with wrist flexors against a preload. When the motor unit firing was

steady, a position profile template was pmented on the oscilloscope. Attempting to match

the position template, the subject stopped resisting the load such that the load extended the

wrist at the approximate velocity of the position template. Tbree different velocities of

lengthening contractions were performed with approximately ten trials of each condition.

The constant load that was held by the subject was either provided by gravitationai weights or

by a constant current fed to the torque motor. In the latter case, even though the current was

constant, the load during wrist extension was not. For these experiments, genenlly, quite

high threshold units were studied. Because of friction in the system, a small preload would

not extend the wrist. High velocities of lengthening contractions could be achieved only with

large preioads, and hence, higher threshold units.

2. Impmed load lengthening contractions. The subject performed an isomeûic

contraction against a constant background load provided by the torque motor. Then an

additionai ramp load was imposed on the background load. During the imposed load, the

subject w;is asked to try to maintain a constant level of motor unit activity in the muscle

throughout the lengthening conttaction. Because the increased load was not matched by

increased muscle contraction, the increase in load impsed a lengthening contraction on the

31

subject. The dope of the tamp load was changed which led to a range of corresponding

angular velocity of lengthening contractions. A step Uicrease in load produced a very fast

lengthening contraction by stretching the active muscle very quickly. Step loads used for

these experiments were very small, and hence produçed very small wrist extensions. Small

step loads were essential for recording discemible motor unit activity.

Data Analysis

Dara analysis were dune off-line on a Pentium 200 PC computer. The data

recorded on VCR cassette was transferred to ihe computer wich the Cambridge Electronic

Design (CED) 1401 Plus computer interface and Spike2 software. The SMU activity, the

position, the tension, the flexor EMG and the extensor EMG were filtered, arnplified and

outputted to tfie computer to be captured on separate analog (waveform) channels. Motor

unit activity, discriminateri by two in series BAK window discriminators, produced transitor-

transitor logic (TïL) puises corresponding to targeted motor units. The 'ZTL pulse for the

targeted SMU and the trigger for the computer were recorded on wparate event (+) channels.

Figure 6 illustrates tbe set-up for data analysis. The SMU analog and the SMU-TTL data

were compared to ensure correct discrimination of the action potentid. TIL pulses from

action potentials that were missed by ihe discriminator were added and extraneous TTLs

were deleted h m the event market record.

In order to examine the behaviour of rnotor unit firing during kngthening

contractions, several parameters of the motor uaits, lengthening contractions and paradigms

were generated using scripts written for the SPKE2 software. Table 1 surnmarizes the

parameters that are subsequently described in the text.

DATA ANALYSIS

Oscilloscope a

Y 1401 Plus Interface 30Hz-3 KHz Cornputer I

1401 Plus Interface Cornputsr

Oscilloscope

2 BAK

Vetter PChl Recorder

Fienor W I) Oscilloscope

Pbsition ~sciiloscope

Vetter PCM Recorder Amplifier

1401 Plus lnterface Computer

Conditionhg Amplifier

-

k

Vettw PCM Recorder

IOOHz-IOKHz

üi i iminntors

Figure 6: The set-up for dûta analysk of single motor unit, SMU T lL extensor EMG, position and tension.

-

1401 Plia Interface 30Hz-3KHz Cornputer

-

Tension I) Osciiioscope

140 1 Plus tnterface Cornputer

Vetter PCM Recorder

Conditioning Amplifier

- h

1401 Plus Interface DC Cornputer

- 4 Conditionhg Amplifier

Table 1: Summary of the parameters generated for each motor unit and for each individual lengthening contraction.

. .

MUTA Motor unit isomeûic recruiûnent threshold

1 Isometnc relative recniitment order I

1 1 Mean angular velocity 1

Lcn*ning contraction

Motor Unit Triggered Average: During movement, the geornetric relationships between the

muscle fibres and the needle electrode can change and, thus, affect the waveform of a motor

unit (Desmedt, 1% 1). SMU action potential shape and size were not always completely

reliable in consistently tracking and identifying a particular SMU. In order to track a motor

unit throughout the lengthening contraction and distinguished it from other moior units which

may have a similar shape, a motor unit triggered average (MUTA) was generated using spike

triggered averaging between SMU-ITL pulses and the unrectified surface flexor EMG. The

MUTA of an SMU stays constant while the shape of rnicmlectrode recorded SMU potential

frequently changed with movement. This aided in identiwng the single motor unit

throughout the lengthening contraction.

Motor unit ncniitment and firing pattern Mean rectifiai surface EMG activity

, ~otai cimges in tension Angular diplacement

Isometric Recruitment Ordec The absolute isometric recniihnent threshold for a motor unit

was determined using isometric voluntary contraction. Starting with a relaxed muscle, the

subject recruited single motor units by slowly increasing the isometric tension. The level of

tension at which a motor unit dischargeci tonically was defined as its isometric cemitment

threshoid. The absolute recruitment thresholds values were calculaîed as tension values and

34

as a percent of the maximal voluntq contraction (5% MVC). The absolute isometric

recmitment threshold was unable to be determined for many rnotor units. In sucb cases the

relative isometric reccuitment order was determined for a pair (or group) of motor units. This

included classiQing the motor units as lower or higher threshold unÎts according to the

relative rank order in which they were recruited during the isometric contraction.

Motor unit recnritntent andfiring pttern: Numerous experiments have established the

orderly recruitrnent of motor units according to the size pn'nciple during isometric

contractions (Milner-Brown et al. 1973b; Henneman and Mendell, 198 1). The corollary is

that if recniitment (or derecruitment) of motor units during lengthening contractions mimics

that of isometric contraction, Iengthening contractions can also be said to foIlow an orderly

recruitment according to the size principle. Establishing the isometric tecruitment order

allowed for cornparison to the lengtheaing contraction recruitment, and thus characterization

of the motor unit recruitment and firing patterns during the lengthening contraction. When

the absolute nor relative isometn'c recruitment order of the motor units could not be

established, the lengthening contractions could not be used because the recruitrnent strategy

for lengthening contractions could consequently not be detennined.

Surface EMG: Quantification of the surface EMG was performed to d o w for cornparisons

of population fiexor EMGs between the isometric and tengthening contractions. The flexor

surface EMG activity was quantifiai by rectifying the EMG signal and dekrmining the mean

integrated EMG values of 200 ms before and 200 ms after the start of the lengthening

contraction. For each motor unit king snidied, correspondhg mean integrated EMG values

35

were averaged for one type of lengthening contraction. Cornparison between tbe mean

integtated EMG values for the two intervals were made using a two-tailed, paired t-test with

a significance ciiffierence reported at a level of p 5 0.05.

Total changes in tension: D u h g lengthening contractions, there was a change in tension

values. Figwe 7 shows the tension trace for a typicai example of both the constant Lod and

imposed load lengthening contractions and illustrates the direction of change in tension

during constant load and imposed load Iengthening contractions. The totai change in tension

started at To and ended at Tm~.

Angular displacement und velocify: Figure 7 illustrates the position values used for angular

displacement and velocity for the constant load and imposed load lengthening contraction.

The angular position values at the start of lengthening contraction (Po), after 100 ms (Piw),

200 ms (PZoo), 500 ms (Pm), and at the end of the lengthening contraction (PEND) were

obtained to calculate the angular displacements at respective time interval. For constant load

lengthening contractions, the start of initial decrease in tension signifîed the start of the

lengthening contraction, and for imposed load lengthening contraction, it was the start of the

increase in tension. A total lengthening contraction was defineci h m the initiai change in

tension until the last change in position. The mean angular velociity of tbe wrist was

calculated using the angulu displacerrient of the wrist divided by change in time. To

compare lengthening contractions of different duraiions and Iengths, the angular velocities

were cdculated after 100 ms, 200 ms, 500 ms and for the totai Iengthening contraction. The

I I

Tension I I 1 t I I I I I 1 I

Position I I I

I Tension I

I

I I 1 I I I

Position I I I

PO! ey x

I

! Extension

Flexion

Extension

Flexion

Eîgarc 7 Drawing of typical examples of consiant a d im@ Ioad lengthening contiactions pceceded by an isomeaic contraction. The position values at the times (t) indicated are used CO caldate ihe angular displacement after lOOms (PIm- Po), 2lXlms (Pm- Pd, 500ms (Pm- Po), and the total position change of the lengthening contraction (Pw> - Po). They are a h used ta calculate the mean angular velocities a i k 100nis ((Piao-P0)Ço.l~) 200ais ((Pm- Pm.2s), HlOms ((Pm- Po}105s), as well as the mcan angular velacity of the total lengthening conaacricm ((PEND-Po)/(tm- ta}). Tbe iod change in tension is detennined by Tw - TO.

range of the velocities of lengthenhg contractions is important in establishing cornparisons of

velocities to other studies.

Ail lengthening contractions were preceded by an isometric contraction. At

least 1 tonicaily firing motor unit, and up to as many as 5 discemible single motor units, were

held f h g in the background during the isometric phase before the start of the lengthening

contraction phase. For each set of lengthening cantractions, one motor unit action potential

was targeted and tracked throughout the set by discrimination to a Tmt pulse. However, the

recruitment and firing pattern of al1 discemible motor units recorded dong with the tracked

motor units was followed in order to establish the recruitment order of the motor units. The

subject received audio feedback only on the targeted motor unit.

Data are presented for 70 tracked single motor units recorded h m tbe flexor

carpi radialis of six subjects. Absolute isometric recruitment thresholds were obtained for 10

out of 70 motor units establishing a range from 110 g up to 646 g (2% to 11% MW).

Absolute isometric recruitment thresholds of other units were not available, however the

preloads used for recruitment of other units were similar, leading to a comparable range of

motor unit thresholds. Furthemore, motor units with relatively high recmitment thresholds

were studied for constant load lengthening contractions because in or&r to elicit high

velocity Lengthening contractions, a large preload was necessary to achieve a strong initial

isometric contraction.

With a targeted motor unit firing in the background, the subjects performed a

mean of 20 (range h m 3 to 88) lengthening contractions. At any one template velocity or

level of background activity, 3 to 12 lengthening contractions were completed for a tracked

motor unit. A total of 500 constant load lengthening contractions were perfonned with 35

tracked single motor units wbich were isolated during isometric contractions. Of these 35

units, 20 tracked single motor units were studied with gravitationdy loaded lengthening

contractions, and 15 were studied with constant current loaded lengthening contractions.

556 imposed load lengthening contractions were executed with 36 different tracked single

motor units, and 33 1 step pulse load lengthening contractions were observed with 9 different

cr;tcked single motor units. Frequently, there were additional motor units recorded

simultaneously with the targeted motor units mentioned above. The presence of these other

motor units was essential to draw important conciusions about motor unit behaviour during

lengthening contractions because they aiiow for a recruitment order to be establisbed between

different motor units.

Angular Diplacements and Mean Anplar Velocities

Resuits of recruitment order and firing pattern of motor uni& depend on the

velocity of the lengthening contraction (Nrudone et al., 1989; Kossev and Chnstova, 1998).

The experiments were designed to cover a wide range of velocities. The angular

displacement (change of wrist position) after 100 ms, 200 ms, and 5ûû ms h m the start of

the lengthening contraction (defined as the initiai change in tension) were computed. Figure

8 shows the fiequency disiribution of angular displacement of the wrist represented by the

degrees of wrist extension afcer 100 ms, 200 ms, and 500 ms for the constant Ioad

lengthening contractions including both gravitational and constant current loads. Figure 9

shows the same for the imposed load lengthening contractions. Both figures iiiustrate similar

ranges of anguiar displacemeots. 1t is important to note that even though a subject was

ptesented with t h position templates to foliow, subjects found template tracing dift?cult,

40

*~ngular Displacement aïter 200ms

*Angular Displacement alter SOOms

I 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 5 Angulir Displitement (degremm)

- .-.

Figure 8: The frequency distribution of the mgular displacement during consant lond lengthening contractions. Change in wrist position after Iûûms, 200ms, and 500rns is displayed.

80 -

* ~ n ~ u l a r Dlrplacemanl alter 2OOmr

+Angular Dlsplacrmrnl alter zooms 60

Angulir Displrcement (drgraes)

Figure 9: The frequency distribution of the angular displacement during imposed load lengthening contractions. Change in position d e r 100ms, 200ms, and 500ms is displayed.

particulady during constant load lengchening contractions. This led to a wide range of

velocities of lengthening contractions.

The mean angular velocity was derived from the total change in angular

displacement over the t h e period. Because of enormous diffecences in background loads,

and sensitivity of the potentiometer, onset of displacement vacied considerably. Therefore,

average displacement over 100 ms, 200ms, and 500 ms per unit time were taken as estimates

of velocity of lengthening. The mean angular velocities obtained from the position data in

degrees per second during the initial 100 ms, 200 ms, and 500 ms of the constant load and

imposed load lengthening contractions are depicted in figures 10 and 1 1, respectively.

Angular velocities by differentiating the position trace were not calculated because the rate of

change of angular displacement was very non-lineu, thiit is lengthening did not occur at a

constant velocity.

-r-FhlAnglarvqaikgfiiriiaMnr

-tMoenAnglarv~&IirignR1SOOrs

5 10 15 P 2 5 3036 40 4 5 5 0 5 5 a6570 75 80 85 90 96lCû106110 m m k g u l r i h b d l y ( ~

Figure 10: The frequency distribution ofthe mean angular velocity during constant load lengthening contractions. Mean angular velocity during the Grst IOOms, 2OOms. 500ms is displayed.

+Mean Angular Velocity during lirst 100ms

-x-Mean Angular Velocity during first 200ms

+Mean Angular Velocity during first SOOms

M i i n Angulir Viloclty (drgr~irlsicond)

Figure 11: The frequency distribution ofthe mtrui angular velocity of imposcd load lengthening contractions. Mean angular velocity dwing ihe first IOOrns, 200ms. 500ms is displayed.

Angular displacements ofgreater tban 2 degrees of wrist extension and mean

angular velocities greater than 5.0 degrees per second, are plotted in figures 8,9, 10 and 1 1.

Smaller displacements and velocities were ciassifieci as very slow and were omitted from the

graph for clmity. Lengthening contractions that were completed before LOO ms, 200 ms or

500 ms did not have displacement or velocity values for any subsequent tirne priods. The

figures show a continuum of angular dispiacements and velocities of the lengthening

contractions, which indicates the wide range of lengthening contractions performed during

the expriment.

In terms of the entire lengthening contraction of constant and imposed load

conditions, starting from a flexed wrist position the total angular displacement ranged h m

appmximately 1 to 52 degrees wiih a mean of 25 &gcees. Figure 12 shows the frequency

43

O 2 4 6 8 10 121416 1 8 2 0 2 2 2 4 2 6 2 8 3 0 3 2 3 4 3 6 3 8 4 0 4 2 4 4 4 6 4 8 5 0 5 2 toid -a Dkpla#mnt (ckqom)

Figure 12: The frequency distribution of the toial mgulru dispiiiccment of the lengthening conmctions.

distribution of the total angular displacement during the iengthening contraction. Figure 13

shows the frequency distributions of the mean angular velocities for al1 of the lengthening

contractions including the constant load and the imposed load lengthening contractions. The

mean angular velocities for the total lengthening contractions ranged from approximately 0.2

to 128 degrees per second. This was caiculated fmm the total position change divided by the

total time of completion of the lengthening contraction, Constant load lengthening

contractions had a range h m 0.2 to 124 degrees per second. imposed load lengthening

contractions had a range ftom 0.3 to 128 degrees per second. The velocities for the total

lengthening contraction are usefiil for description of the lengthening contraction as weii as

cornparison purposes to the velocities used in other studies. Lengthening contractions were

divided into slow and fast lengtfiening velocities. The classifications consist of slow

44

&Constant Load *lmposld lood

1 Total Angular Vmlocity (dmgrmsshmcond) Fi yn 13: The frequency distribution of the total angular velocity for the lengthening contractions.

lengthening contractions included velocities below approximately 35 degrees per second and

fast lengthening contraction included velocities pa te r than 50 degrees per second, and in

between they were considered medium velocity lengthening contractions. The classification

is not discrete nor absolute, but simply an approximate range of velocities in whicfi

lengthening contractions exhiiited similar characteristics.

Constant Load Lengthening Contractions

P r e l d

The preloads during the gravitational loaded lengthening contractions ranged

from 130 g to 1000 g correspondhg to approximately 2% to 17% of the maximum voluntary

contraction, The prehads imposed by the toque motor during a constant current lengthening

contraction cange h m 125 g to 750 g (2% to 13% MW). Through variation of the I d , a

range of muscle forces inciuduig different amounts of motor units could be æcruited.

Tension and Position

The start of ii constant Load lengthening contraction was characterised by a

distinct decrease in the tension exerted by tbe subject. Dunng a typicd slow lengthening

contraction, the dec~ase in tension continued slowly and graduaily throughout of the

lengthening contraction. However, during the fast lengthening contractions (generally p a t e r

thsin Wh), a biphasic shape in the tension trace was observed. Fit, an initial decrease in

tension occurred to allow for wtist extension followed by an increase in tension presumably

to slow and stop the lengtbening contraction. Even though the position trace showed a

rnonotonic extension of the wrist, the tension trace showed a biphasic shape. The upper trace

in Figure 14 shows a typicd example of this shape. The relationship of position and tension

is important in understanding the firing patterns of motor units during lengthening

contractions. The tension pattern gives insight into the motor unit recniitment and ring

pattern during lengthening.

Single Motor Unit Responses

M e n the subject with a tonicaily ïJring motor unit(s) dowed the background

load to extend the wrist, three generai patterns of motor unit discharge were observed during

repeated lengthening conu~~:tions: (1)the toaic motor uni@) silenceci during ihe lengtheoing

contraction, (2) the tonic motor unit(s) contiaued to fire during the lengthening conuaction,

46

1

Figure 14: Tension and position traces of a constant gnvitational load lengthening conîriwion illusîrating the biphasic pattern of tht tension trace during fast lengthening contractions. The angular velocity of the lengthening conuaction is approximately 8501s (pb405).

and (3) initially the tonic motor unit(s) is silenced, then midway through the lengthening

contraction, the same unit(s) tlred.

The predominant firing pattern of single motor units during constant load

lengthening contractions showed a silencing of the tonically firing motor unit(s) in the

background. Figure 15 shows a typical example of a constant load lengthening contraction

opposed by a gravitational load (A) and a constant load lengthening contraction opposed by a

torque motor load (B). Out of the 35 motor units studied during the constant load

lengthening contractions, 28 motor units exhibited the pattern of complete silencing of motor

units during the lengthening phase. 37% (186 out of 500) con lengthening contractions, 186

or 37% exhibited this behaviour. The time of occurrence of the silencing vacied, it could start

right at the onset of the initial decrease in tension or any time during the lengthening

Figure 15: Typical results h m constant load lengihening conûactions paradigm showing the silencing of the tonic single motor uni& (A) This figure shows 3 tonic motor units (1 large and 2 smali plus additional very small units) king silenceci during a gravitationd load lengthening contraction. The large, higher threshold unit was the tint unit to be demiteci. Note the large oscillations in the tension trace and the pasition trace during the slow contraction of 36" in -1.6s (22Smfs) (pb5OS). (B) This figure shows 3 tonic motor units (1 large and 2 smali) king silenccd during a constant cumnt load lengthening contraction. Again, oscillations, though l e s proncninced, are seen in the tension and position traces of this slow contraction of LCP in - 1.4s ('7%) (mg 105). Traces ftom top to bonom, flexor EMG, tension. position, SMU are displayed, An upwards change in the tension trace indicate-s an increase in tension and a downwards change indicates a demûse Extension is shown by an upwards change in the position trace aiad flexion is shown by a downwards change. The vertical bar indicates the beginnjng of îhe lengthcning conimtion.

contraction. S o m lengtfiening contractions showed an abrupt silencing or derecniitment of

alL tonic motor units whiie others showed a progressive orderly derecruitment of motor units.

When more than one unit fïred during the isometric contraction, the large motos units were

derecruited before small motor units as seen in Ggwe 15.

The second pattern of lengthening contractions with constant I d showed a

continued firing of the motor unit(s) in ihe background. Continued Firing of the motor units

included variation in the number of units that sustained activity. In some cases al1 tonic

motor units continued to Fm and in ohers higher threshold motor units were derecruited

while the small motor units continued as is iiiustrated in figure 16. The pattern of continued

firing motor units was seen in 20 out of 35 motor units. and uccurred during 30% (150 out of

500) of the constant load lengthening contractions. Generally, if a motor unit continued to

fre throughout the entire constant load lengthening contraction, the mean firing rate of the

single motor unit would decrease until the singie motor unit cesised to F i or the lengthening

contraction ended.

While many of the constant load lengthening contractions involved e i h r a

complete or partial silencing of the single motor units, there were many lengthening

contractions that exhibited a temporary silencing of single motor unit(@ and then ph& re-

recruitment of the same mit(~). This ttiitd pattern of single motor unit firing o c c d with

21 motor units during 32% (158 out of HIO) of the constant load lengthening contractions.

Figure 17 illustrates atypical example. The recruitment after silencing of the motor units

during the lengthening contraction occurred at various times ranging h m approximate1y 150

to 300 ms. The phasic recniitment of the motor unit@) was associated with an inctease in

tension which was decelerathg the lengthening phase. Also, during this phasic firing of

49

Figure 16: Typical results from constant load lengthening contractions paradigm showing the continuation of the single motor unit açtivity, (A) This figure shows 2 tonic motor uni& (1 large lower thnshold and 1 small higher thrcshold) continuing throughout a gravitational load lengthening contraction. Note the oscillations in the tension and the position traces in this slow contraction of 375" in -2.5s (15%) (pb712). (B) This t7gure shows 4 tonic motor units (1 large higher thnshold and 3 srnall lower thrcshold) of which the large unit is cieredted early in the lengthcning contraction while the small motor unie continue to tire until the end of the constant c m n c load lengthening contraction. The contraction is 6" in -15s long (4%) (kj 14). Traces €rom top to bottom, fiexor EMG, tension, position. $MU are displayed. An upwards change in the tension trace indicaies an increase in tension and adownwards change indicsites a decrease- Extension is shown by an upwards change in the position trace and flexion is show by a downwards change. The vertical dashed bar indicates the beginning of the lengthening contraction.

i?ipre 17: Typical results from constant load lengthening contractions paradigm showing the re-recruitment of tonic single motor units that were dereccuited at the beginning of the Iengthening contraction. (A) This figure shows 2 clear tonic motor uni& and additional small background motor units (1 large higher ihreshold, 1 unit of medium size) during a gravitational load lengthening contraction, The medium sized unit and small uni& continue to tire throughout the lengthening contraction while the large unit (mow) is te-ncnùted a k r an interval of -3OOms h m the îùst dec- in tension. The total position change is 40" in 400111s (10Ws) (pb72 1)- (B) This figure shows 4 tonic motor units (1 large higher thnshold and 3 small lower threshold units) d k n g a constant cunent Ioad lengthening contraction. The units are silenced at îhe onset of the lengthening contraction and the small units ( m w ) are rc- m i t e d during the middle of thc lengthening contraction at a time of -150ms from the initiai derrease in tension. The total contraction o c c d over 11" and lasted 150ms (73'1s) (kj141. Traces are similar to those displaycd in previous figures. The vertical bar indicates the beginning of the lengthening contraction.

motor units during lengthening contraction, a phasic burst of surface EMG was observed

which presumably contributed to the increase in tension and bcaking of the wrist extension.

The important points to note are that the unit firing phasically during lengthening in figure

17A is ihe same unit which was firing in the background. Secondly, while the large unit

derecmited, the lower threshold, smaller contractions units continued to fire during the

lengthening contraction. In figure 17B, only the smailer, lower threshold units fired

phasicaiiy, and the large one did not. No additional units were recruited.

Surface EMG

in the literature, it has been suggested that due to selective recruitment

of larger units, EMG during lengthening contractions is higher than during isometric

contractions (Nardone et al., 1989). To evaluate this ünding, the surface EMG

recorded fmm wrist flexors during the controlled isometric contraction was cornpared

to the lengthening contraction for each set of units recorded during constant load

conditions. The vaiues for the integrated EMG for al l the different lengthening

contractions are included in Table 2. The table Iists the mean surface EMG for 200

ms before and after the onset of the lengthening contraction for 35 motor units.

Paired t-test showed a statistically signïficant decrease in mean integrated EMG

during the lengthening contraction. Figure 18 shows a typical example of the EMG

activity. During the isometnc contraction for period of 200 ms before the lengthening

contraction, a mean EMG activity of 83.65 fl was observed and during the fkst 200

ms during Iengthening contraction that value dropped to 6.36 p.

Table 2: Mean surface EMG for constant load lengthening contraction (LC).

Unit # 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 1 8 19 20 2 1 22 23 24 25 26 27 28 29 30 3 1 32 33 34 35 M m

Variance

(cc: constant curent, gr: gravitational)

M u n EMG fa Before LC

Figure 18: A typical example of the EMG activity during a constant load lengthening contraction. The top tnce shows the rectifiai EMG (pb405). Traces from top to bottom, rectified FCR EMG, FCR EMG, tension, position. comcted FCR SMU are displayed. An upwards change in the tension trace indiates an inm;ise in tension and a downwards change indicates a decrcasc. Extension is show by an upwiuds change in the position trace and flexion is shown by a downwards change. The mean EMG amplitude 200 ms before and after the start of the lcnglhcning convacrion are indicated above the rectifiai EMG trace. The 3 vertical bars indicate 200 ITE before thc s t u t of the Iengthening contraction, the beginning of the lengthening contraction and 200 ms &et the lengihening contraction respectively.

Unusual Single Motor Unit Firing and Recruiîment Patterns

In a few isolated cases, unusual patterns of motor unit recruitment occurred.

For a total of 6 out of 500 (1%) constant load lengthening contractions from four different

units, single motor unit rec~itrnent pattern during lengthening differed from the orderly

recmitment (or derecniitment) pattern. Figure 19 shows an example when a new, Iarger

higher threshold motor unit that h d once duRng the lengthening contraction whiie none of

the background units Wd. But for the same background activity, 17 additional lengthening

contractions at different speeds did not recniit tbis unit again.

Figure 19: An example of an unusual panern of m i t m e n t during the constant load lengthening contractions pandigm. The figure shows 4 tonic motor units (2 large higher ihnshold and 2 small lower thceshold units). A new large unit is n c ~ i t c d during the lengihening contraction (pbl6). The totai contraction occurred over 15" and lasted 1.8 s (8 "Is). Traces h m top to bottom, FCR EMG, tension, position, FCR SMU are displayed. An upwards change in the tension trace indicates an increase in tension and a downwards change indicates a demase. Extension is shown by an upwards change in the position trace and flexion is shown by a downwards change. The vertical bar indicates the beginning of the lengthening contraction. In a t o d of 18 lengthening contractions npeated on these motor units, thii pattern was seen only once.

Oscillatory behiour

Imgularities in the form of oscillations in the position and tension traces were

evident dwing the lengthening contractions. The amplitude of the oscillations varied and

were generally dependent on the velocity of the lengthening contraction. Large oscillations

were observed in the tension traces for slower, pmlonged lengthening contractions. Figures

15A and 16A illustrate the pmnounced slow oscillations in tension seen during the decrease

in tension. Oscillations are noted in figure 15B although they are of quite smaller amplitude.

The oscillations are seen to be relatively absent for fast lengthening contractions. For

example, figures 17A and 17B show only very small oscillations in the tension and position

record. Frequencies of the oscillations ranged from 3 Hz in figure 16A to 8 Hz in figure 19.

Imposed Ramp h d Lengthening Contractions

Preloarls and Imposed Ramp Loads

The preloads applied by the torque motor varied from 125 g to 750 g (2% to

13% MVC) at 10 cm. The ramp load that was superimposed on the preload was aiso

ptoduced by the torque motor and vacied in the camp increase of speed and magnitude.

These ranged fiom 250g to 750 g. The total preload plus the load never exceeded 1000 g

(iimited by capacity of the torque motor),

Tension and Position

The start of an imposed load lengthening contraction was characterised by an

increase in net tension. The tension trace continued to increase during the lengthening

contraction as the load imposed on the subject increased. Slow irnposed load lengthening

contractions developed tension very slowly and fast lengthening contractions showed a rapid

rise in tension. The change in the tension trace was dependent upon the subject's resistance

to the increase in imposed load. This voluntary resistance led to a variety of different

patterns. The position record appmximately traced the tension record with a slight delay.

Figure 20 illustrates a typical example of the tension and position traces for a fast wcist

extension. The top trace shows the tirne course of change in force with accompanying

extension of the wrist joint.

Single Motor Unit Responses

The subject contracted wrist flexors isometrically against a background load.

An additional load was superirnposed to extend the wrist joint producing a lengthening

contraction of the active wrist flexors. The goal for the subject was to try to maintah a

constant level activity so as to allow the increased load to extend the wrist. In a few

I Figure 20: Tension and position traces during an imposed load lengthening contraction. ~Gical incre;ises in ten&n and position are An. The velocity of the contraction is appmximately 54"/s (pM0 1).

experiments step pulse loads were also superimposed to lengthen the actively contracting

wrist flexors. However, only a litnited number of trials were perfonned for two reasons.

First, such a study has been previously done in detail (Calancie and Bawa, 198Sa) and,

second, step loads that produced comparable wrist extensions as in the other conditions

produced very strong reflexes. During such strong reflex activity clear distinguisbable

motor units could not be recorded and thus the firing and rec~itment pattern could not be

detemiined.

The imposed load lengthening contractions showed large variability in the

single motor unit responses, some were similar to patterns observeci wiih constant load

lengthening contractions, the magnitude of the load and the camp speed of the load. The

patterns were largely dependent upon the subject's voluntary response to the imposed loads.

The three typical firing patterns during imposed load lengthening contractions included (1) a

decreased firing rate andlot silencing of the tonic motor unit(s), (2) a continuation andor an

increase in the firing rate of the motor unit(s), and (3) recniitment of additionai higher

threshold unit(s).

The first pattern of a constant load lengthening contraction showed a decrease

in firing rate andior a silencing of the firing of the motor unit@) in the background. Figure

2 1 is a typical example of the silencing of motor units during such conditions. The pattern

of decreasing rate or silencing of the background firing motor units was seen in 6 out of 36

motor units and occurred during 10% (56 out of 556) of the imposed load lengthening

contractions. In the example shown in figure 21, it cm be seen that during lengthening a l l

motor units are derecniited, the larger before the mal1 ones which would be expected

according to the sue principle.

Figure 21: Typical resulu from imposed load lengthening conuactions paradigm showing the silencing of the tonic motor units. This figure shows 4 tonic motor units (1 large and 3 small) plus additional very smail uni& k ing silenceci midway through a lengthening contraction. The large, higher thnshold unit was the first unit to be derecruited. Note the small oscillations in the tension trace during the contraction of 36" in -800111s (45%) (pb409). Traces of FCR EMG, tension, position, FCR SMU are displayed respectively from top to bonom. An upwards change in the tension trace indicates an increase in tension and a downwards change indicates r demase. Extension is shown by an upwards change in the position trace and flexion is shown by ûdownwiuds change. The vertical bar indicates the beginning of the lengthening contraction.

The predominant f ~ n g pattern of single motor units during imposed load

lengthening contractions was a continuation of the r i n g of the tonic motor unit(s) in the

background according to the instruction given to the subject. Figure 22 is an example of a

recording in which the subject maintained some motor unit activity. The large higher

îhreshold unit was derecniited, but the small lower threshold units continued to fire

throughout the lengthening contraction. Figure 23 provides two additional examples of the

continuation of motor units with slightly different patterns during lengthening contraction.

Ali background units continued to tire thughout with slight lengthening of interspike

Figure 22: Typicd resutts fiom imposed load lengthening contractions paradigm showing the continuation of single motor unit activity. This figure shows 3 tonic motor uni& (1 large higher threshold and 2 small lower threshold) with the derdtment of the Iiuge motor unit and the continuation of the smdl units throughout the lengthening contraction which displaces 22.5" in -800ms (28%) (kj45).

intervals. 32 motor units during 64% ( 372 out of 556) of the imposed load lengthening

contractions exhibited the continuation of motor units nring pattern.

The last generai pattern of single motor unit firing occurred with 16 out of 36

motor units during 24% (133 out of 556) of the imposed load lengthening contractions.

Figure 24 is an example of additional motor units king recruited during the imposed load

lengthening contraction. The recniitment of additional motor uni& during the lengthening

contraction occurred at various rimes throughout the imposed load lengthening contraction.

This pattern of recruiûnent was during both slow and fast Iengthening contractions. Note that

the lower threshoId uni& continue to 6re as higher threshold unit was recruited.

Figure 23: Typical results from imposai load lengthening contractions paradigm showing the continuation of single motor unit activicy over two difirent specds. This figure shows 5 tonic motor units (1 large highcr thrcshold and 4 small tower thmhold) with a demase in the firing rate of the large motor unit is seen during Iengthening contraction which displaces 400. The lengthening contraction times are (A) 1s (40'1s) and (B) 500ms (8001s). Note the tension and position osciilations in slow contraction (pb714). Traces from top to bottom. FCR EMG, tension, position, FCR SMU are displaycd. An upwards change in the tension tnce indicates an inctease in tension and a downwards change indicaies a decteosc. Extension is shown by an u p w d s change in the position Irace and flexion is show by adownwards change. The vertical bar indicates the beginnhg ofthe lengtkning conaction.

Figure 24: Typical results from imposed Ioad lengthening contractions pandigm showing the recniitment of additional single motor units during h e lengthening contraction. This figure shows 1 small lower threshold tonic motor unit with the additional larger threshold motor units appearing mid-way through the Iengthening contraction. The total position change is 12" in -1.1s (1 1'1s) (mg103). Traces ftom top to bonom, FCR EMG, tension, position, FCR SMU are displayed. An upwards change in the tension trace indicates an increiise in tension and û downwards change indicates a dwrease. Extension is shown by an upwards change in the position trace and flexion is shown by a downwards change. The vertical bar indicates the beginning of the lengthening contraction.

Su#ace EMG

During imposed load lengthening contractions, if the subject tried to maintain

the same activity before and during the lengthening contraction, surface EMG should be

comparable during the two periods. Table 3 îists the mean integrated surface EMG for 28

units 200 rns before and after the onset of the hposed load lengthenhg contraction. Using a

paired t-test, the mean EMG values of ail mirs 200ms before and d e r the start of the

62

lengthening contraction were compared. Paired t-test showed a statisticaüy signincant

decrease in mean integrated EMG during the lengthening contraction. However, note much

more variability was seen, as 10 units showed an increase in activity during the lengthening

contraction and 26 units showed a decrease. Figure 25 illustrates an example of the integrated

EMG of an imposed load lengthening contraction. During the isometric contraction for

period of 200 ms before the lengthening contraction, a mean integrated EMG activity of

46.04 pV was obse~ed and during the first 200 rns during lengthening contraction that value

was 50.00 pV. Note that the mean integrated EMG value over the first 400 ms of the

lengthening contraction did increase to 86.34 pV.

ilnusual Single Motor Unit Finng and Recruitment Patterns

As was seen during the constant load lengthening contractions, unusual

patterns of motor unit recruitment occurred during imposed load lengthening contractions. in

9 out of 556 (2%) imposed ioad lengthening contractions of five motor units exhibited

patterns of recruitment that differed h m the orderly recruitment (or derecruitment) patterns.

Figure 26 shows an example of a large bigher threshold motor unit f i n g during the

lengthening contraction and the smalier motor unit ceased to Fm. Twelve lengthening

contractions were perfonned with this set of motor units at this approxirnate velocity and 2

out of the 12 lengthening contractions showed this type of phasic recniitment. Since phasic

recruitment is probabilistic, 2 out of 12 daes not qualify for reversed recruitment. Most

imponantly, the large unit was not a vecy large twitch motor unit caused by the selective

recruitment of large units. It was just the next higher threshold unit as shown in figure 24. It

just happened to 6re only once.

Table 3: Mean surface EMG for imposed rmp load lengthening contractions (LC).

Unit # 1 2 3 4 5 6 7 8 9 10 1 1 12 13 14 15 16 17 18 19 20 21 22 23 24 2s 26 27 28 29 30 3 1 32 33 34 35 36

Mean Variance

Before LC 16.77 21.51 67.20

. 52.51 57.25 57.90 92.75 68.87 73.3 1 90.79 78.70 62.77 72.02 169.43 15 1.69 40.10 34.60 40.74 33.01 1 1.79 2 1.69 39.04 24.46 18 -43 30.12 12-77 11-70 8.98 4.05 8.25 11.64 10.66 7.86 7.87 6.45 6.50 40.88 1604.79

NOTE: 10 units showed an increase in activity during the lengthening contraction. 26 showcd a decrcase

Mean EMG for

I

[-Test: Paired Two Sample for Means t Stat 323 PVc=t) two-tail 0.00256 t Critical two-tail 203

200 ms (pV) Dunng LC

23.92

II

I -

u 100 ms

Figure 25: A typical example of the EMG activity during an imposed load lengthening contraction. The mcan ampütude of EMG for a typical i m p d toad 200 ms bcfore and 200 ms after the start of the lengthening contraction determinui fÎom the f i t decnasc in tension are shown in the boxes (pb803). Nom. This pwticular example wouid pmbably show a significant increasc in the mean iEMG if the time uscd for integration was expanded,

C---(

100 ms Figure 26: An example of recruinnent of a largcrthrshold unit during an imposed load lengthening contraction. The smallet, Iowa thrrstiold unit ceases ta tire and a large unit was recruitcd. Howevcr. very srnaIl uaiis do contiaue to fm in background. Fmm the EMG trace, it is evident that a large burst of muscle activity o c c d at the time of the large motor unit firing and the smaller unit may be cefractory and ihus unable to fire (pb6û6).

Oscillatory Behaviour

As was seen in constant load lengthening contractions, oscillations were

evident in the tension and position traces during imposed load lengthening contractions.

Slow lengthening contractions, such as in figure 23A. showed distinct oscillations in both the

tension and position trace. Faster lengthening contractions showed significantly smaller

osciliations as seen in figure 24.

Imposed Step Load Lengthening Contractions

Square puises, 150 ms in duration fed to the torque motor, extended the wrist

joint producing small fast camp lengthening contraction of wrist flexors. These lengthening

contractions had small angular displacements of 1.5 to 6 degrees. These displacements are

small, although similar to some lengthening contractions that were completed in the otber

two conditions. These displacements are not comparable to displacements used in the

Literature. However, the muscle is king actively lengthened. Such fast stretches elicit strong

stretch reflexes. As shown previously by Calancie and Bawa (1985a), a size-ordered reflex

recruitment during the rapid stretch was found. The tonic background single motor units

tended to respond during both the shoa latency reflex (30-55ms) and the long latency reflex

(55-100ms) periods and additionai larger units which were the next higher threshold units to

be recruited through voluntary effort. Figure 27A shows background tonic units firing dwing

the stretch reflex with an additionai larger unit responded during the long latency reflex

period. This large unit is just the next unit to be recruited voluntarily as shown in figure 27B.

The unit was recniited to fire tonicaüy and the loads were irnposed to examine aU tonic

rnotor units.

Figure m. Typical results h m ttsestep iuque pulse imposed load lengthening contraction. (A) This figure shows 4 tonic motor units (1 large and 3 small). During the step toque pulse lengthening contraction, a new h g e higher thrrshoId motor unit is recruited -65111s after the beginning of the toque pulse. The other background tonic units also fire concumntiy (pb14). (B) In the same expcriment, ihe large moior unit which fired phasically in A, is recniited to be tonic to increase the total to 5 tonic uni& (2 large and 3 small). Now. during the step torque pulse, a decreasc in the inter-spike inmval is secn with the large motor unit fuing again at -60111s aftcr the application of îhc toque pulse(pb 14). Traces, ftom top to bottom, comsponding to FCR EMG, tension, pition, FCR SMU are diiplayed. An upwards change in the tension trace indic- an i~xease in tension and a downwards change indicates a decrease. Extension is show by an upwards cbange in the position trace and flexion is shown by a dowawards change. The vertical bar indicates the beginning of the lengthening contraction.

EMG Tremor

Thmugh a visuai inspection of the data, a noticeable trernor in the surface

EMG was observed before and during many lengthening contractions. Figure 28A and 28B

show typicai examples of this phenomena. The slight tremor was seen in selected recordings

of aimost al1 the subjects across al1 threshold motor unit(s). Subjects experienced muscle

tremor for brief periods while they were holding a constant force and/or d u ~ g the

leagthening contraction. The trernor is depicted as bursting of EMG activity made

increasingly evident with rectification as in figure 29, In many cases, the tremor was

accompanied by brief periods of synchronous finng of single motor unit. It was found that

the tremor was increasingly evident during later sets of lengthening contractions or usuaily

during or following lengthening contractions with large preloads probably resulting in fatigue

of the muscle.

Summary of Motor Unit Firing Behaviour

Dunng the lengthening contractions of the human FCR, an orderiy

recruitment or derecruitment of motor units according to their relative voluntaty isometric

threshold was seen during approximately 98% of the lengthening contractions. There was no

evidence to support systematic selective recruitment of large, fast-twitch motor units with a

derecniitment of the smail, slow twitch units. Constant and imposed load lengthening

contractions of different velocities gave a variety of different patterns, but the large majority

of units exhiiited recniitrnent and 6ring patterns bat were in accordance with the size

principle of orderly recruitment. When Iarge motor uni& were recruited, they were generdy

the next highest threshold motor unit to be recruited with isometric voluntary effort.

Figure UI: An example of the accentuoted amor during a lengthening contraction. (A) Bursts are seen in the surface EMG and are emphasized in the rcctified signal. The single motor unit activity shows king bursts of single motot units during the lengthening conuaction. Synchronization ofunits may possibly be occwring which is evident from the random finng of motor units during the initiai isometric periad, and bwsts of xtivity during the lengthening contraction. Nok that the large motor uni& do not firr done, but they accompanied by smder units. Traces, h m top io bottom, corccsponding to FCR EMG, tension, position, FCR W aie displayed, An upwards change in the tension trace indicates an increase in tension and a downwards change indicales a demase. Extension is shown by an upwards change in the position trace and flexion is shown by a downwards change types of lengthening contractions. The vatical bar indicates ihe beginning of the lengthening conaaction.

Figure 29: An example of amor during an imposed load lengthening contraction (pb408). The rectified FCR EMG makes the tremor quite apparent. Traces, fiom top to bottom, correspondhg to rectified FCR EMG, FCR EMG, tension, position, FCR SMU are displayed. An upwards change in the tension m e indicates an increase in tension and a downwards change indicates a decrease. Extension is shown by an upwards change in the position trace and flexion is show by a downwiuds change, The vertical bar indicates the beginning of the lengthening contraction.

DISCUSSION

The purpose of this study was to characterize the recniitment and firing

pattern of motor units during lengthening contractions. To accomplish this the isometric

recruitment order of al1 discernible motor units was determined, with the lower and higher

threshold units defined according to either their isometric reccuitment threshold or theu

relative recniitment order during the isometric contraction. In generai, the recniitrnent of

motor uni& during lengthening contractions of the wrist flexon was shown to follow the

recmitment of motor units during isometric contractions. The absence of selective

recniitment of large, higher th~shold motor units during the lengthening contractions of the

flexor carpi radialis strengthens support for the size principle of m i t m e n t of motor units.

Limitations of the study

The success of single motor unit experiments is dependent on correctly

tracking individual motor units with the a h of determining their firing and recniitment

pattern. Several trials did not meet the discrimination criteria and were discarded during

recording or were not included in the analysis. The exact success rate of the experiments was

unavailable because on-line analysis revealed the motor units during several lengthening

contractions were indistinguishable and thus were not recordai for M e r off-line anaiysis.

In total 70 motor units were tracked during a total of 1056 constant and imposeci load

lengthening contractions which we believe gave us an adequate sample for detennining the

recruitment pattern of motor units.

Perfonning single motor unit experiments is not a simple task. It requires

7 1

subjects who are able to conirol the intensity of their muscle contractions so that individual

motor units can be identified wMe performing the necessary experimental procedure.

Therefore, skilled subjects are required which results in a small number of subjects during

single motor unit experiments. In our study, only 6 subjects were involved. Yet, aii the

subjects in our study did produce the sarne generai patterns of firing of motor units and we do

not believe this produce any biases in the data. In addition to the number of lengthening

The establishment of the motor unit recruitment during lengthening

contractions relies on the validity of the cornparison between the recruitment of motor units

during isometric and lengthening contractions. We believe this to be true because an orderly

recruitment of motor units according to the size principle has clearly been determined during

voluntary isometric contractions of muscles (Milner-Brown et al., 1973b; Monster and Chan,

1977; Yemm, 1977; Calancie and Bawa, 198% Thomas et al,, 1987; Riek and Bawa, 1992;

Jones et al., 1993). Since the order of recniitment for isometric contractions was considered

as the control, only those sets of single motor uni& where the isometric recruitment order was

established were included in the study for Iengthening contractions.

Recording of motor unit activity during movements can result in the variation

of the shape and amplitude of the action potentials due to the movement of the electrode with

respect to the muscle fibres. Because of variations, careful visual inspection of the motor

units or generation of MUTA was necessary to correctly identify the motor units. Even

though, the change in size and sbape of motor units often occurred during the lengthening

movement, the firing of the unit couid be foUowed h m one motor unit action potential to the

next because the change was usually gradual through the lengthening contraction. In many

instances, the original size and shape returned wkn the wtist was retunied to the original

72

position. However, some data was unable to be inclukd in the study because movement of

the needle made it impossible to establish identity of the unit under investigation.

The delimitation of the study rats on the generalizability of ihe flexor carpi

radialis to other human muscles. Oae might question whether certain muscles, wbich might

experience rapid lengthening contractions frequently during behavioural movements, are

more prone to the selective recruitment of large motor units. Although lengthening

contractions of the flexor carpi radialis do not readily occur, the biceps brachii does

reoccuringly experience rapid lengthening contractions and in three studies using this muscle,

no selective recruitment was observed. We believe that with a more thorough study, like the

one presented hete with the flexor carpi radialis, the triceps surae will be shown to follow an

orderly recmitment according to the size pcinciple. However, in an attempt to compare motor

unit recruitment strategies across muscles, it is important that the muscle possess sirnilar

input ihrough neural connections. The flexor carpi radialis and the triceps surae muscle do

possess similar central nervous system connections, including Renshaw cells and

heteronymous connections. It is also difficult to compare parameters such as contraction

velocities across different muscles because of different muscle properties including muscle

length, architecm and fibre type composition. We attempted to control for the ciifferences

between muscles in order to compare between muscles, but acknowledge that comparisons do

have restrictions.

Anguiar Disphcement and Velocity

Comparison of the velocities and position changes obtained in this siudy to

other studies reveals that a sufficient range of angular displacements and anguiar velocities

73

were performed. The relative relaxation times of motor units in the individual muscles were

considered. The slowest relaxation tirne of motor units of the triceps surae occurs in the

soleus muscle which has a relaxation time of 500 ms (ref). In the study by Nardone et al.,

ankle extensor lengthening contractions were performed at approximately 25 degrees of ankie

flexion in 1 second, which is approximately twice the relaxation time of the slow soleus

motor unit. The flexor carpi radialis has a fast relaxation time of 100 ms. Therefore, an

analogous velocity is 25 degrees in 200 ms for a final velocity of approximately 100 degree

per second. Approximately 30 lengthening contractions were performed at velocities above

100 degrees per second. Therefore, we believe comparable velocities were performed.

However, as described above it is dificuit to compare contraction velocities across different

muscles so we attempted to cover a large range in order to include any velocities where

selective recruitment in the flexor carpi radialis may occur.

It must be mentioned that comparison of angular displacements, angular

velocities and the percent of maximum voluntary contraction between studies using different

muscles is limited due to many factors. For example, one could postulate whether the

excursions of the wrist flexors in this study is comparable to that of the uiceps surae in the

study of Nardone et al. (1989). Normai range of motion at joints could be compared, but that

still does not take into account the differences in original muscle lengths, changes in muscle-

tendon ratios or muscle moment arms.

It is dificuit to compare magnitudes of angular velocities because of different

muscle properties, including lengths of the muscles being studied. As weii, the other studies

used the statt of the change in position as the start of the lengthening contraction, where in

our study the start of the change in tension was defmed as the start of the lengthening

contraction. Therefote, surne disctepancies in the exact velocities may occur* To overcome

the potentiai restriction, the ideal strategy was to cover a wide range of velocities. In

addition, if accordhg to Nardone et al. (1989), selective d t m e n t occurred only in a

certain range of velocities then it was necessary to test the entire range of velocities. in our

study a large range of velocities were completed. Specifically, the range of velocities

comparable to that useci during other studies we covered was from and no velocities showed

a tendency for large motor units to be recruited selectively.

Single Motor Unit RQCtlljtment and Rring Pattern

Our results showed no evidence of s y s t e d c selective mniitment of large

higher threshold motor units with derecruitment of small lower threshold units. The vast

rnajority (98%) of the discrirninated motor units was recruited in order of tecruitment

increasing size. Subjects performed two types of lengthening contractions of the wrist

flexors. During the different lengthening contractions, many variations of firing patterns

were observed. The firing pattern during the lengthening contraction usually involved a wide

variety of recmitment, derecruitment and increasing or decreasing firing rates of motor units,

but none of the Iengthening contractions violated the size principle of motor unit recruitment.

Comporison of the Ibo opes of Consîant Load Lengthenhg Conhacnions

The gravitationaily loaded and the constant current l d e d lengthening

contraction revealed no significant difference in the pattern of their lengthening contractions.

Traces for each type of lengtheaing contraction showed the same gened patterns, which is

evident in the similar figures. Both types also have a similar range of velocities of

contraction. The central nervous system does not distinguish the type of load (wbether

gravitational or peoduced by toque motor) that stretched the active muscle, only the effect of

the applied load is apparent.

Constani Lm&

During some slow lengthening contractions, the angular displacement of the

wrist extension was smooth with derecruitment of background units. The derec~itment

occurred at various times during the lengthening contraction, but no additional remitment

was seen dunng this derecruitment. However, often when a subject petformed a slow

lengthening contraction, the angular displacement was not smooth as it was superimposed by

slow oscillations as shown in figure 21. The same phenomena can be seen in the figures of

the studies by Howell et al. (1995) and Nardone et al. (1989). Perhaps îhese slow oscillations

which include very small, fast shortening or isometric contractions akin to ballistic

contractions would recruit a burst of low and higher threshold motor units. The tension

traces in our study frequently showcd small increases in tension similar to small

superimposed ballistic shortening contractions during which some recruitment of motor units

were seen. Most of the motor units were the same motor units that had been tonically firing

in the background. Additional rec~ited units were those detennined to be the next highest

threshold and not selected large, higher threshold units. However, the Nardone et al. (1989)

study did not report any tension records for their lengthening contractions and thus

cornparison is unavailable.

During fast lengthening contractions with constant load, most of the tnds

showed a silencing of aü the motor activity during the lengthening contraction. At the start

76

of lengthening contraction, tension decreased with simultaneous decrease in motor unit

activity. This was foUowed by a fast increase in tension, while the wrist was still extending.

The biphasic shape of tension, illustrateci in figure 21, may explain the sudden re-recruitment

of same motor units such that in or&r to stop the lengthening contraction as it nears the end

of the required displacement, the muscle contracts and recmits motor units to consequently

end the lengthening contraction. Therefore, fast lengthening contractions repeated saw an

orderly recruitment of the same lower threshold motor units ihat were noted during the

isometric contraction. This is contradictory to the suggestion by Nardone et al. (1989) that

large motor units would be recmited in order to provide a fast relaxation time during the fast

lengthening contraction. The motor units that were recruited in our study had a sufficiently

short relaxation time to produce the rapid lengthening contractions

Imposed Ramp LwdP

When an active muscle was lengthened by an additional ramp, again an

orderly recruitment was obsewed with no systernatic selective recruitment of large, higher

threshold motor units over small, lower threshold units. During lengthening contraction with

slow imposed ramp loads, background units generally continued to fire with no additional

units recruited. The tension increase was usually very slow as weU. With fast imposed ramp

loads, additional units were fquently recruited, though not at the expense of derecruitment

of lower threshold units that were tonically firiag in the background. These additional

recruited units were the next highest threshold units recniited ituough voluntary recniitment.

The tension inctease during the lengthening contractions was due to the resistance of the

imposed ramp load, ibis was also generally associated with increased fîring of the motor unit.

77

The imposeci load displayed more variability in the recruitrnent pattern of its units due to the

higher possibility of response of ihe subject. It depends on a balance between how much a

subject lets their wrist be extended versus how much they resisted voluntarily.

With slow ramp increase, we did not observe recruitment of additional units.

With faster camps very frequently we observed pbasic firing of additional units. These

additional units, again, were the next higher threshold units tested either with voluntary slow

or ballistic contractions. It may also be noted that the burst of additional units was most

probably due to fast voluntary reaction of the subject. The motor units fired at approximately

200 to 250 ms after the onset of the imposed ramp load. This time is much longer than the

time for reflexes (25-100 ms). With fast imposed ramp loads, additional units were

frequently recmited, though not at the expense of derecruitment of lower threshold units that

were tonically firing in the background. These additional recmited units were the next

highest threshold units recniited through voluntary recmitment (Figure 27).

Imposed Step Loadr

The lengthening contractions in our study that were produced with step ramp

loads showed an orderly recruitment pattern. This corresponds to results established during

the thorough study by Calancie and Bawa (1985a) on motor unit recruitment during imposed

step loads on the wrist flexors tbat demonstrated that recruitment proceeds in an orderly

fashion according to the size principle through the production of the stretch reflex.

Surfaœ EMG

During lengthening contractions with constant loads, the surface EMG of the

78

wrist flexors showed a decrease in activity in our study. This is contrary to the increase in

surface EMG during lengthening contractions reported by Nardone et al. (1989). However,

in accordance with our results, Moritani et al. (1988) and Kossev and Christova (1998) did

not observe an increased surface EMG during the lengthening contraction. Both reported a

decrease in EMG activity pointing to tlse efficacy of lengthening contractions due to the

mechanical stiffness of the muscle. During lengthening contractions with irnposed loads, in

our study the surface EMG was generally lower. The instruction given to the subject was to

maintain a constant level of activity in the muscle, but variability in the response of the

subject to the irnposed load causes fluctuations in the surface EMG activity, but overall,

EMG was significantly lower during lengthening contractions. This confinns the efficacy of

lengthening contractions that has been reportecl in the literature such that under comparable

work loads, the electrical activity recorded involved in lengthening contractions is less than

that involved in the shortening of muscles (Bigland and Lippold, 1954; Basmajin, 1967;

Bigland-Ritchie and Wood, 1976). This lower recorded electrical activity at any given force

is achieved with either fewer fibres actïvated or lower frequencies of discharge or a

combination of both (Stauber, 1989).

Bursts in surface EMG activity accompanied by synchronous firing of motor

units occurred during several trials. The oscillations observed in the EMG of our study

developed either during trials involving relatively high loads like those incurred during the

gravitational loaded lengthening contractions or following these bigh load trials whüe

performing irnposed load lengthening contractions. This is consistent with involuntary

physiological tremor. Synchtonization of discharge of motor units can occur when an input

to the motoneuron pool is sufficiently large @ietz,et al., 1976), which occurs with

contractions that required large amounts of force (Jessop and Lippold, 1977). With increasing

fatigue and especially tremor brought on by fatigue, motor units tend to fire synchronously

(Milner-Brown et al., 1973a). The EMG bursting and the synchronization of motor units

were not quantifiai due to the limited and sporadic occurrences of the phenomena But

whatever the cause of the supposed trcmor, îhe recruitment and firing pattern of the motor

units did not violate the size principle.

Random Reversals of Recruitment Order

In our study, 2% of lengthening contractions showed a reversal of the

remitrnent order in motor units. These reversals occurred between motor units that were

rec~ited successiveiy during voluntary isometcic contractions and, thus, were sirnilar in their

recruitment thresholds. Reversals can d l y occur with motor units of similar conduction

velocities or twitch contraction times. Nomally in motor recruiünent studies, reversals occur

for less than approximately 10% to 15% of trials (Henneman and Mendell, 198 1). These

reversals do not have serious functional consequences due to the evidence that reversals

occur between motor units with similar properties (Senn et al,, 1997), and thus will not

interfere with gradual force production. Howeli et al. (1995) suggested a systematic selective

recruitrnent order with a 14% (3 out of 21) rate of reversal of motor units. Two of the three

units in their study could be better interpreted as recniitment revetsals between motor units of

similar thresholds. The one other motoc unit might betîer be explained through the

probabilistic f ' n g of motor units (Jones et al., 1994). Furthemore, this probabilistic firing

does not provide evidence for a theory of selective m i t m e n t of motor units during

lengthening contractions, but is a random phenornenon.

Selective Recruitment

Selective recruiûnent of motor units implies more than the random

recruitment reversai of motor units wiih similar thresholds like that seen in the HoweU et al.

(1995) or a random firing of a motor unit, but it involves the deactivation of the lower

threshold smail motor unit dong with recmibnent of a normally higher threshold large motor

unit. This was show by Kanda et al. (1977) wiih electrical stimulation of sural nerve in the

cat. Surai nerve stimulation inhibits slow S type motoneurons and excites F type

motoneurons. With a smng synchronws stimulation of sural nerve selective recruitment

was seen in triceps surae muscles.

In our study, large motor units were not selectively activated during

recruitment. Nardone et al. reported rnotor units that would fire during the lengthening of

active muscles and were silent during shortening and isornetric contractions. We believe that

the data from Nardone et ai. (1989) can be explained by Zengthening contractions with

irregularities in their position traces caused by small ballistic contractions occurring during

the lengthening phase. Therefore, the units that were said to be recruited only during the

lengthening phase were actually tecruited during mal1 isornetric or shortening contractions.

Even though we argue against selective m i t m e n t within the same muscles,

shifting of activity between different muscles is possible and observed. The synergistic

activity between muscles performing a task is not in question. For example, a shift of

recnlltment of motor units from soIeus (a slow, single joint muscle) to gastrocnemius (a fast,

two joint muscle) may mcur between hese spergistic muscles during a specifîc task such as

walking or nuining. This shifting of activity feom soleus to gaswnemius has been noted in

8 1

the literatuce (Nardone and Schieppati, f 988). However, shifting of activity from one muscle

to the next does not support a selective tecIuitment pattem because it is the recmitment order

of motor units within a muscle that is important, This shifting between different muscles

with different properties could not be confimed in the forelimb muscle because properties

(including speed of contraction) of all forearm muscle are quite similar.

Input to the Motor Udîs

The muscle activation pattem for isometric and dynarnic voluntary

contractions originates frorn commands of the central nervous system. if isornetric,

shortening and lengthening contractions are controlled through different command inputs to

the motoneurons as some would suggest (Nardone et al., 1989; Enoka, 1996), then an active

muscle producing one type of muscular contraction, for example, an isornetric contraction,

which changed to another contraction, for example, a lengthening contraction, should display

a change in the motor units recruited. However, our results showed the same motor units

recmited consistently during both the isometric and lengthening contractions, although with

different firing patterns. This suggests similar, but different levels of excitatory input to the

motoneurons depending on the specific type and level of contraction.

Possible mechanisms complicating the performance of lengthening

contractions and the variation of position, tension and motor unit activity during the

lengthening contractions may be expIained by additional input h m muscle afferents,

including muscle spindles, due to muscle Iengîh changes. Sensory output h m muscle

spindles can be generated by stretching the muscle. During lengtheniag contractions, small

itregular changes in angular displacements associated with uninteaded acceleration of a

82

lengthening movement can cause an i n c r e d discharge h m spindle endings (Burke et al.,

1978). These spindle responses can be associated with adjustments in the discharge pattern

of the voluntarily activated mucor units at latencies corresponding to the operation of spinal

reflex mechanism (Burke et al., 1978).

From a functional point of view, the size principle is a logical and economical

way for the central nervous system to control force production (Henneman and Mendell,

198 1). The size principle of orderly recniitment simplifies the neuromuscular control by

reducing the degrees of fieedom of the newomuscuhr system (Cope and Clark, 1995). For a

given level of signal descending to the spinal cord, an appropriate number of motoneurons

are recruited with suitable properties to carry out the desired movement. At higher tensions,

because the motor units are generally composed of larger muscle fibres and larger number of

muscle fibres, their tension increments are still appmximately the sarne proportional increase

in the total tension already present at the tirne of their recruitment (Henneman and Olson,

1965; Binder et al., 1996). Derecruitment from large to small motor units then would also

lead to an incremental decrease in force and as a result fine control can be possible at al1

tension levels.

Conclusion

The purpose of the study was to gain better understanding of the recruitment

of motor units during lengthening contractions. Our results show that during lengthening

contractions, flexor carpi radialis motor utiits are d t e d and detecniited in an orderly

manner according to the size principle and selective recruitment of large, higher threshold

motor units during lengthening contractions does not occur. Although cornparisons are doue

83

between muscles, further study needs to be done with the triceps surae muscles in order to be

able to directly investigate lengthening contractions that are comparable to those performed

during the study by Nardone et al., 1989. We suggest h m our results that the studies which

have ciaimed selective recruitment during lengthening contractions may have rnisinterpreted

their data. Lengthening contractions in Our study did not show selective recruitment of

motor units suggested by Nardone et al. (1989) and Howell et al. (1995). Our results support

the recruitment patterns reported by the previous results of Moriani et al. (1988), Sogaard et

al. (1996) and Kossev and Christova (1998).

Since the motor unit is the final conunon pathway for motor cornrnands, the

recruitment and firing pattern of the motor unit can provide insight into the complex

organization of the neural control of movement. Knowledge of how the human

newomuscular system controls the activation of a muscle during lengthening contraction has

applications in many areas. Particularly, due to muscle king actively lengthened in many

normal activities illustrated by the presence of lengthening contractions in movements such

as walking, running, jumping and throwing, just to name a few.

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