Key words: neuromuscular compartment; skeletal muscle; functional electri-SHORT REPORTcal stimulation; innervation; morphology

MUSCLE NERVE 20: 897–899 1997

NEUROMUSCULAR COMPARTMENTSIN THE LONG HEAD OF TRICEPS: AMORPHOLOGICAL STUDY IN RABBITS

JIE LIU, MD, 1 V. PREM KUMAR, MBBS, FRCS,1* HUI-KING LAU, BEng,1

BARRY P. PEREIRA, MEng,1 YAN SHEN, MD,2 and

ROBERT W. H. PHO, MBBS, FRCS1

1Department of Orthopaedic Surgery, National University of Singapore, Lower KentRidge Road, Singapore 1192602Department of Hand & Reconstructive Microsurgery, National University Hospital,Singapore

Accepted 15 January 1997

Mammalian skeletal muscles may consist of two or Schiff (PAS) staining for glycogen4 was performed inone of the limbs of 16 rabbits divided into threemore separate subdivisions known as neuromuscular

compartments,1,4–7 which can be defined as a segment groups, as outlined in Table 1. The opposite limbused as the control was similarly exposed surgicallyof the muscle innervated by a primary, natural, dis-

sectable extramuscular nerve branch to the muscle.4,6 but without denervation of the muscle.The rabbits were maintained for 2 weeks to ensureSubsequent studies have suggested that there might

be anatomical and functional features unique to the glycogen depletion within the denervated muscle seg-ment. Then, both the experimental and control mus-neuromuscular compartment.3,6,7,18,19

In this study, a detailed morphological analysis of cles were harvested and their weights recorded. Eachmuscle was divided into 12 equal cross-sectionalthe rabbits’ long head of triceps was conducted to

determine the innervation pattern, volume, fiber blocks and quick frozen in liquid nitrogen. Fromeach block, a cross section of 25-mm thickness wastype distribution, and motor end-plate zone of each

of its neuromuscular compartments. taken and stained with PAS.The glycogen-rich, glycogen-depleted, and total

cross-sectional areas were then digitized. The volumeMATERIALS AND METHODS

Distribution of Intramuscular Nerve Branches (n 5 24 was estimated by V 5 O12

i51A(i)t, where V is the

Muscles). Muscles with their extramuscular nervebranches were dissected, harvested, and stained using volume, A the cross-sectional area, and t the thick-a modified Sihler’s technique17 to demonstrate their ness. The volume of the denervated segment wasintramuscular nerve branching pattern.

corrected for atrophy by addingMc 2 Me

McVT to it,

Volume (n 5 32 Muscles) and Muscle Fiber Typing where VT is the total volume and Mc,e are the masses(n 5 8 Muscles). Under anesthesia, the three termi- of the control and the experimental muscles, respec-nal nerve branches to the muscle were identified. A tively.partial denervation of the muscle with periodic acid- In eight of these muscles, sections were taken and

stained with myofibrillar adenosine triphosphatase(ATPase)8 for muscle typing. Five randomly selectedfields of each compartment with a total 150–200 mus-

*Correspondence to: Dr. V. Prem Kumarcle fibers were examined under 4003 magnification.Contract grant sponsor: The National University of Singapore; Contract

grant number: RP950330; Contract grant sponsor: National Medical Re- Type IIa and type IIb fibers were not differentiated.search Council; Contract grant number: NMRC/0066/1995; Contract grantsponsor: Shaw Foundation; Contract grant number: GR05988N

Motor End-Plate Zones (n 5 8) Muscles). The mus-CCC 0148-639X/97/070897-03 1997 John Wiley & Sons, Inc. cles were divided into 12 equal transverse blocks and

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Table 1. Percentage volumes of glycogen-rich and glycogen-depleted compartments and percentages of type II muscle fibersin each compartment in the long head of triceps in rabbits.

Type IImuscle fiber

Volume of Volume of Volume of proportion inCompartments Nerve branch(es) glycogen-depleted glycogen-rich compartments compartmentsstudied Group denervated compartment (%) compartment (%) (mean 6 SD) (%) (mean 6 SD) (%)

Proximal 1a Proximal (n 5 4) 37 60 6 18 (n 5 6) 92 6 2 (n 5 8)717476

1b Middle and distal (n 5 2) 3965

Middle 2a Middle (n 5 3) 13 17 6 4 (n 5 5) 86 6 2 (n 5 8)1522

2b Proximal and distal (n 5 2) 1522

Distal 3 Distal (n 5 5) 24 28 6 4 (n 5 5) 72 6 4 (n 5 8)27273032

the motor end-plate zones were stained according ponded to a main intramuscular branch distributedto a defined segment of the muscle. This gives cre-to Koelle.9

dence to the concept of associating each extramuscu-lar nerve branch with a compartment.4,10 Further-RESULTSmore, denervation of these extramuscular nerves ledDistribution of Intramuscular Nerve Branches.to glycogen depletion of the corresponding compart-Three main intramuscular nerve branches extendingment, implying that each extramuscular nerve inner-from three extramuscular terminal branches fromvated a certain volume of muscle and that this couldthe radial nerve were demonstrated in three-dimen-possibly be differentially activated and may have dif-sional detail. The proximal intramuscular branch al-ferent functions. Electrical stimulation of these differ-ways innervated the largest segment, followed by theent extramuscular nerves resulted in different seg-distal and middle branches. The arrangement of thements of the muscle contracting.12,13,15three parts was from the proximal–dorsal to the dis-

Of the three compartments, the proximal wastal–ventral on the muscle belly.the largest in this muscle. This suggested that theproximal compartment has the largest work ca-Volume and Muscle Fiber Typing. The volume ofpacity.2,11each neuromuscular compartment was expressed as

The proposition that neuromuscular compart-a percentage of the whole muscle (Table 1).ments can have different composition of muscle fiberThe muscle fiber type was predominantly type IItypes3,16 was verified. The proximal compartment con-(Table 1). Of the three, the proximal compartmenttained the highest proportion of the powerful typehad the highest proportion of type II muscle fibers,II fibers11 (92 6 2%) and should be the one mostfollowed by the middle and the distal.suitable for functional electrical stimulation to gener-ate powerful elbow extension. Unfortunately, itMotor end-Plate Zones. Only one zone of motor

end-plates was observed as an obvious band in the would be the fastest to fatigue also.muscle. The motor end-plates were located in the Although the proximal compartment was largermidpoint of the muscle fibers. The motor end-plates than the distal, a previous study13 revealed no signifi-appeared continuously throughout the muscle with cant difference in force generated at the elbow byno discrete innervation bands to differentiate the these two compartments. Markee and Lowenbach15

compartments. have shown that in a two-joint muscle the proximalcompartment acts primarily on the proximal joint,

DISCUSSION while the distal compartment acts on the distal. Ifthis is truly the situation for effective elbow extensionThe long head of triceps in the rabbit has been dem-in functional electrical stimulation, the one electrodeonstrated to have three neuromuscular compart-

ments. Each extramuscular nerve branch corres- should then be placed on the nerve branch to the

898 Short Reports MUSCLE & NERVE July 1997

4. English AW, Letbetter WD: Anatomy and innervation patterndistal compartment, although it is smaller than theof cat lateral gastrocnemius and plantaris muscles. Am J

proximal, because it acts more directly on elbow joint. Anat 1982;164:67–77.5. English AW: An electromyographic analysis of compartmentsHowever, further study is needed.

of cat lateral gastrocnemius muscle during unrestrained loco-The three compartments did not show a discretemotion. J Neurophysiol 1984;52:114–125.

motor end-plate zone to each, contrary to previous 6. English AW, Weeks OI: An anatomical and functional analysisof cat biceps femoris and semitendinosus muscles. J Morpholsuggestions,7,18 indicating that a discrete motor end-1987;191:161–175.plate band is not an essential characteristic for a

7. Galvas PE, Gonyea WJ: Motor-end-plate and nerve distributionneuromuscular compartment, although this might in histochemically compartmentalized pennate muscle in the

cat. Am J Anat 1980;159:147–156.be a finding in some skeletal muscles.8. Johnson MA, Polgar J, Weightman D, Appleton D: Data onThe study of motor end-plate zones and their

the distribution of fiber types in thirty-six human muscles: andistribution in skeletal muscles may have relevance autopsy study. J Neurol Sci 1973;18::111–129.

9. Koelle GB, Friedenwald JS: A histochemical method for localiz-when segments of muscle are harvested in free mus-ing cholinesterase activity. Proc Soc Exp Biol Med 1949;70:cle transfer, as during animation procedures for fa-617–622.

cial palsy.14 It becomes important not only to harvest 10. Letbetter WD: Influence of intramuscular nerve branchingon motor unit organization in medial gastrocnemius muscle.the innervating nerve and blood supply to the muscleAnat Rec 1974;178:402.segment, but also to include the motor end-plate

11. Lieber RL: Skeletal Muscle Structure and Function. Baltimore,zone for optimal action. Williams & Wilkins, 1992.

12. Liu J, Retnam L, Lau HK, Pereira BP, Kumar VP, Pho RWH:Neuromuscular compartments have distinct ana-A rabbit muscle model for studying contraction characteristicstomical and physiological properties which are begin-of muscle with multiple motor points. Muscle Nerve 1994;

ning to be understood. Our morphological study may 17:1477–1479.13. Liu J, Lau HK, Min WX, Pereira BP, Kumar VP, Pho RWH:hopefully be extended to skeletal muscles in pri-

Contractile characteristics on electrical stimulation of musclemates, and the findings there may then be translatedwith multiple motor points an in vivo study in rabbit. Clin

to man. Orthop 1995;313:231–238.14. Manktelow RT, Zuker RM: Muscle transplantation by fascicu-

lar territory. Plast Reconstr Surg 1984;73:751–755.The authors would like to thank Associate Professor E. H. Yap of15. Markee JE, Lowenbach H: The relations between multiple

the Animal Holding Unit for the use of the facilities. innervation and segmental response of skeletal muscle of thedog. J Neurophysiol 1945;8:409–420.

16. McIntosh JS, Ringqvist M, Schmidt EM: Fiber type compositionof monkey forearm muscle. Anat Rec 1985;211:403–409.REFERENCES

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