Recruitment of motor units in human flexor carpi ulnaris

354

Brain Research, 602 (1993) 354-356 (0 1993 Elsevier Science Publishers B.V. All rights reserved 0006-8993/93/$06.00

BRES 25520

Recruitment of motor units in human flexor carpi ulnaris K.E. J o n e s a, p. B a w a a and A.S. M c M i l l a n b " School of Kinesiology, Simon Fraser Unicersity, Burnaby, BC (Canada) and ~' Clinical Dental Sciences, Unicersity of British Columbia, Vancoucer, BC (Canada)

(Accepted 27 October 1992)

Key words: Motor unit; Recruitment; Size principle; Flexor carpi ulnaris

In 1949, Denny-Brown reported that the motoneuron pool of the human flexor carpi ulnaris (FCU) muscle was fractionated into subpopulations, each subpopulation being activated during a different voluntary motor task. The following report presents data on motor unit recruitment in the human FCU muscle for the tasks of isometric flexion and ulnar deviation, cocontraction of the forearm muscles and non-isometric flexion of the wrist. These observations show that every FCU motor unit tested reliably, contributed to all four tasks, that is, no separate subpopulations were observed for any of the contractions tested. Furthermore, the order of recruitment was the same for all four tasks.

D e n n y - B r o w n reported observing the recruitment of separate subpopulations of the h u m a n flexor carpi ulnaris ( F C U ) muscle for different m o t o r tasks. The tasks tested were flexion and ulnar deviation of the wrist, and grasping. It is true that most of the m a m malian limb muscles are activated during multiple tasks or contractions, leading to m o v e m e n t s in different directions. This, however, should not necessarily imply that the m o t o n e u r o n pool of each of these multifunctional muscles is fractionated into subpopulations, thereby, making a subpopulation responsible for each particular task. Fractionation has been reported for some muscles 3'5, but it does not seem to hold true for two of the four main extensor and flexor muscles of the h u m a n wrist, namely, flexor carpi radialis ( F C R ) and extensor carpi radialis ( E C R ) 5. Based on DennyBrown's 1 observations, the question arises, is the spinal cord organization of h u m a n ulnaris muscles quite different from the synergistic radialis muscles? To answer this question, the following experiments were carried out on five healthy h u m a n subjects (2 males, 3 females, aged 2 3 - 4 8 years). These experiments were approved by the Ethics Committee at Si-

mort Fraser University. For details of the experimental setup and data analysis, see Riek and Bawa 5. Briefly, two fine wire bipolar recording electrodes were inserted percutaneously into the F C U muscle of the subject, making sure that the electrodes were not recording from the surrounding finger flexors, flexor digitorum profundus ( F D P ) and flexor digitorum superficialis (FDS). Surface electromyographic ( E M G ) activity was recorded from F C U and the wrist extensors with bipolar A g - A g C 1 disc electrodes. Activity from wrist extensors was recorded to observe muscle activity during the cocontraction paradigm. The recruitment of m o t o r units was examined for four tasks: isometric flexion and ulnar deviation of the wrist, cocontraction of the forearm muscles (with or without making a fist) and non-isometric flexion of the wrist. Since the F C U muscle is primarily a wrist flexor, all comparisons of the m o t o r unit recruitment order were m a d e with respect to the order of recruitment for isometric wrist flexion. The first observation was that F C U m o t o n e u r o n pool did not exhibit distinct subpopulations for any of the four contractions tested. Every m o t o r unit re-

Correspondence: P. Bawa, Anatomy Department, Cambridge University, Cambridge, CB23 DY, UK. Fax: (44) (604) 7913040.

Reprint requests: P. Bawa, Simon Fraser University, School of Kinesiology, Burnaby, BC V5A 1S6, Canada.

355 ULNAR DEVIATION

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137 65 45

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worthy that, while these two units were recruited with very little total E M G during isometric flexion, they required a very strong effort during cocontraction. The recruitment of FCU units during cocontraction always required a strong voluntary effort indicating that the FCU muscle is not one of the main fixators of the forearm. The strong effort needed to activate FCU motor units during cocontraction may be explained by the fact that shoulder and upper arm muscles are being activated to fixate the shoulder and elbow joints prior to the activation of the wrist flexors. Therefore, the total sense of effort is very high before FCU is activated. Higher magnitudes of surface E M G may be attributed to cross-talk from surrounding muscles which are coactivated with FCU during cocontraction. The large magnitude of surface E M G or strong sense of effort needed to recruit the FCU motor units in question, cannot be assumed to reflect activation of a large number of additional FCU motor units not available during other tasks. Table I summarizes the data for 283 paired motor unit comparisons. The paired data presented in this table were such that their recruitment order for isometric flexion was very stable over repeated contractions. Those motor units which were very close in thresholds, and hence interchanged their recruitment

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Fig. i. Recruitment order of two single motor units (SMU), I and 2, are shown for four types of contractions. Top panel in each quadrant shows the two units with concomitantly recorded surface E M G from wrist flexor (middle panels) and wrist extensor (lower panels) muscles. During each task, the smallest unit, SMU 1, was recruited before the larger unit, SMU 2. Data were sampled at 40-/zs intervals. Each of the calibration bars shown in the second quadrant represents 200/zV for all three panels.

cruited for isometric flexion was recruited during the other three tasks (although, very few motor units could be tested repeatedly for three or all four tasks). We then tested the order of recruitment of motoneurons by paired comparisons. The distinction between two motor units was made on the basis of differences in the size and shape of their action potentials as shown in Fig. 1. The recruitment order of two single motor units (SMU) is shown for the four tasks tested. SMU 1 was recruited before SMU 2 repeatedly for all four tasks. Surface E M G data for flexor and extensor muscles are shown for each task. It is note-

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Fig. 2. Twitch torque versus recruitment threshold for five subjects (different symbols) are shown for isometric flexion and ulnar deviation contractions. In spite of the scatter, the data show a monotonic increase in twitch torque with increasing recruitment threshold.

356 order for flexion, were not tested for other tasks. Table I shows that, for 143 motor unit pairs compared between isometric flexion and ulnar deviation, 137 (95.8%) showed the same order of recruitment. For 49 pairs compared between isometric and non-isometric flexion, 45 (91.8%) pairs had the same order of recruitment. During cocontraction, from a total of 91 pairs, 65 (71.4%) showed the same order while for 16 pairs the order of recruitment could not be distinguished. The recruitment of FCU motor units during cocontraction was difficult and generally abrupt, the pattern being similar to that observed for ballistic contractions. Such recruitment patterns made it difficult to discern recruitment order. Ten motor unit pairs also exhibited recruitment reversals during coeontraction. The above-mentioned observations made on motor unit action potentials reflect the recruitment order of motoneurons in the spinal cord. These do not yield any information on size-related recruitment. Even if they did, size-related recruitment in the spinal cord would not necessarily indicate orderly recruitment in terms of force output. The reason being that the force vectors of different muscle units may contribute different proportions of force components in various directions. In other words, some muscle units may be dominant in one direction while the others may contribute predominantly to another. Hence, for two distinct directions of contraction, isometric wrist flexion and ulnar deviation, we studied the order of recruitment in terms of force output. In each of the two directions, the twitch tension of the recorded motor units was computed by the spike triggered averaging technique 4'5. For all subjects, graphs of twitch torque versus recruitment threshold of FCU motor units were plotted for each of the two isometric contractions and are illustrated in Fig. 2. The data clearly demonstrate a monotonic increase in recruitment threshold with increasing twitch torque for

both directions of contraction. This monotonic relationship suggests an orderly recruitment, from small to large, of the representative population of FCU motor units. (Motor units were sampled up to approximately 75% of the maximum voluntary force of wrist flexion.) The above observations indicate that FCU motoneurons in man are not fractionated into subpopulations for the four tasks examined here. Rather, the whole pool contributes to each of the contractions. Furthermore, the order of recruitment is according to size principle 2 for each of the contractions tested. The differences in our observations from those of DennyBrownl may be due to the fact that the FCU muscle is a very small muscle surrounded by very large finger flexors, F D P and FDS. When recording from FCU, it is important to ensure that the indwelling electrodes are not picking up activity from the surrounding muscles. It is suggested that the separate subpopulations mentioned by Denny-Brown I were not FCU motor units, but possibly belonged to the neighboring muscles. This work was supported by grants from the British Columbia Health Research Foundation and Natural Sciences and Engineering Research Council of Canada to P. Bawa.

REFERENCES 1 Denny-Brown, D., Interpretation of the electromyogram, Arch. Neurol. Psych., 61 (1949) 99-128. 2 Henneman, E., Somjen, G. and Carpenter, D.O., Functional significance of cell size in spinal motoneurons, Z NeurophysioL, 28 (1965) 560-580. 3 Loeb, G.E., Motoneuron task groups: coping with kinematic heterogeneity, J. Exp. Biol., 115 (1985) 137 146. 4 Milner-Brown, H.S., Stein, R.B. and Yemm, R., The contractile properties of human motor units during voluntary isometric contractions, J. PhysioL London, 228 (1973) 285-306. 5 Rick, S. and Bawa P., Recruitment of motor units in human forearm extensors, Z Neurophysiol., 68 (1992) 100-108.