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Neuromuscular compartments in the human biceps brachii muscle R i c h a r d L. Segal Division q[Ph.vsical Therapy, Department of Rehabilitation Medicine. and Department o]Anatomy and Cell Biology, Emor~ University School q[' Medicine, Atlanta, GA 30322 ( USA ) (Received 15 January 1992; Revised version received 10 March t992; Accepted 11 March 1992)
Key wordsv Biceps brachii; Human; Neuromuscular; Compartment; Architecture; lnnervation; Anatomy Electrophysiological evidence suggests that the human biceps brachii muscle is organized into functional neuromuscular compartments. The purpose of this study was to determine whether there was an anatomical basis for these compartments. Dissection of the biceps revealed both architectural and nerve branching pattern compartmentalization within the muscle. Although the biceps brachii is grossly subdivided into long and short heads, these heads are further subdivided into roughly parallel architectural compartments. Moreover, these architectural compartments usually receive a private nerve branch, thus supporting the notion that the human biceps brachii has neuromuscular compartments.
The identification of the peripheral elements controlled by the central nervous system (CNS) to generate movement is controversial. Questions exist regarding the smallest functional elements (e.g. motor units, neuromuscular compartments) controlled by the CNS. Resuits from studies by Letbetter and English [6, 9] demonstrated that the cat lateral gastrocnemius muscle is organized into neuromuscular compartments. Moreover, these compartments can behave differently according to task requirements [5]. Thus, these neuromuscular compartments may be the smallest component controlled by the CNS. For a global perspective of the issue of neuromuscular compartments within muscles refer to the eloquent review by Windhorst et al. [14]. In addition, the terminology used to describe neuromuscular compartments is confusing. This issue is addressed comprehensively by Chanaud et al, [4]. For the purposes of this paper, the term neuromuscular compartment will be used to describe muscle subunits delineated by architecture and nerve branching patterns. Recent investigations from this laboratory have examined anatomical and functional neuromuscular compartments in three human muscles: lateral gastrocnemius (LG), flexor carpi radialis (FCR), and extensor carpi radialis longus (ECRL) [11--13]. Other laboratories studying compartments in human muscle have focused only C))rre,spondence." R.L. Segal, Room 209, Center tbr Rehabilitation Medicine, Emory University School of Medicine, 1441 Clifton Road, NE, Atlanta, GA 30322, USA.
on electromyographic (EMG) recordings and have provided no anatomical basis for their choice of recording sites. Electrophysiological studies by ter Haar Romeny et al. [7, 8] and van Zuyten et al. [15] have demonstrated a topographical organization of the long head of the human biceps brachii that is related to the critical motor unit firing levels for different tasks. Thus, within the long head of the biceps brachii, motor units recorded from lateral locations were recruited for elbow flexion, units recorded from medial sites were recruited for supination or linear combinations of flexion and supination; and more centrally located units were recruited for non-linear combinations of flexion and supination. There is no evidence in the literature to suggest that the human biceps brachii is anatomically organized in a manner that would provide a basis for the results of ter Haar Romeny et al. [7, 8] and van Zuylen et al. [15]. Studies reporting the staining of the biceps brachii using either acetylcholinesterase histochemistry [1] or the binding of [3H]~-bungarotoxin [2] have shown that endplates lie along a strip in the middle of the bellies from medial to lateral, a region whose extent is 5--10 mm from proximal to distal. Surface EMG studies used to map innervation zones also indicate that the motor end-plates lie in a row midway between the proximal and distal bony attachments of the muscle [10]. These studies, however, did not investigate the branching patterns of muscle nerves or the gross architecture of the muscle. Thus, whether the end-plate organization reflects an organization that supports the physiological data of ter Haar
99
B
C
Fig. 1. Photographs of biceps brachii specimens. A: a deep or posterior view of a biceps specimen. The coracobrachialis is attaching proximally with the short head {labeled by number 1). The neuromuscular compartments are clearly visible from this view. In this specimen the nerve branches Io the long (labeled by number 2) and short heads come off directly from the musculocutaneous nerve. Also, notice the crus of the tendon of insertion ~ hich is labeled as number 3. In this photograph left is distal and the top is medial. B: the superficial or anterior view of the same spccimen as in A. Notice th~tt neuromuscular compartments are Hol visible from this view. The superficial view shows how the long head (labeled as number 2) inserts more proximally ~mto the tcndon of insertion (labeled as number I ) than does the short head. In lhis photograph left is distal, the top is latcral and the short head is labeled by number 3. (7: a superficial or anterior vicw of the distal end of another specimen with the samc orientation as B. This photograph shows the more proximal attachment of the long head (labeled by number 3) onto tendon of insertion (labeled as number I). The photograph also shows the short hcnd (labclcd by number 4) attaching more intimately to the bicipital aponeurosis {labeled by number 2) than the long h e a d Both the long and short heads attach to the tendon proper (labeled by number 1}.
Romeny and coworkers [7, 8] remains unknown. The nerve branching patterns, muscle architecture, and their relationship may provide an anatomical basis for the physiological findings [7, 8] of functional neuromuscular compartments in human biceps brachii. Thus, the present work was undertaken to examine whether there is morphological evidence for neuromuscular compart-
ments within the human biceps brachii, particularly its long head. Samples of biceps brachii ( n = 6 : 3 right: 3 left) were obtained from perfused human cadavers donated to the Medical School's Department of Anatomy and Cell Biology. The average age at death was 72 years. Blunt dissection was conducted with the aid of a visor-mounted mag-
I00
nifier (5x) or a dissecting microscope (10-40x) on muscles both in situ and after removal from the cadavers. The courses taken by branches of the musculocutaneous nerve to each muscle and their branches to each head were defined and compared between cadavers to evaluate their consistency. The major branches of each of the nerves were followed as they divided within the muscle until they could no longer be followed at 10-40x. The orientation of the tendons of origin and insertion, and the direction of muscle fibers were also noted while performing the dissection. The muscle fiber direction and points of attachment along with nerve branch relationships were then documented with sketches, photographs and written descriptions. The angles of pennation were not measured in the present study. Muscle fibers were carefully removed as necessary to view the full extent of their tendinous attachments. The drawings in the text reflect typical patterns of architecture and innervation of these muscles. The biceps brachii has long (lateral) and short (medial) heads, The tendons of origin for both heads become broad as they course from proximal to distal and do not end until about the juncture of the proximal one-third and middle one-third of each head, respectively. Muscle
fibers take origin from the deep suri;ace of these broad tendons (Fig. IA). The muscle fibers in both heads arc arranged in parallel along the longitudinal axis of lhc muscle (Figs. 1 and 2). However, there are fl'om two to four natural groupings of the fibers in each head when viewed from the deep surface (Figs. I A and 2A). These groupings will be referred to as the architectural portion of the neuromuscular compartment. The fiber groupmgs are n o t clearly visible from the anterior or superficial view (Figs. IB and 2B). Thus, because most observers only view the superficial portion of the biceps, the presence of the neuromuscular compartments has not previously been documented. The two heads of the biceps 'fuse' just proximal(Figs. 1B and 2B) to the elbow joint, attaching distally to the radial tuberosity of the forearm via the biceps tendon and to the ulna via the bicipital aponeurosis (Figs. lC and 2B: laceratus fibrosis). The lateral compartment of the long head and the medial compartment of the short head attach more distally onto the deep surface of the tendon of insertion (Fig. 2A). The medial compartment of the long head and the lateral compartment of the short head attach more proximally and superficially onto the tendon of insertion (Fig. 2A). In addition, these muscle
B. Anterior or Superficial Surface
A. Posterior or Deep Surface )roximal
-- Short head
nerve
Long head
Branch to long head
head Medial
Lateral Lateral Medial head Short
Crus
Tendon
Tendon of insertion
Distal
aponeurosis Distal
Fig. 2. Drawings of biceps brachii muscle. A: a view of the deep or posterior surface of the biceps. The asterisks demarcate neuromuscular compartments of the long and short heads. The main nerves to the long and short heads do n o t come directly from the musculocutaneous nerve in two-thirds of the specimens, but from the bifurcation of a branch of the musculocutaneous nerve (compare to Fig. IA). Notice that there are usually private nerve branches to the compartment. B: a superficial or anterior view of biceps. The neuromuscular compartments are n o t visible from this view. Notice that the long head inserts more proximally than the short head. The short head is more closely associated with the bicipital aponeurosis which attaches to the ulna.
101 fibers attach along a crus of the tendon of insertion (Figs. 1A and 2A). The fibers from the short head are more intimately linked to the bicipital aponeurosis than fibers from the long head (Fig. 1C). However, the long head does link to the aponeurosis (Fig. 1C). Finally the fibers from the long head attach more proximally to the anterior surface of the tendon of insertion than those from the short head (Figs. 1B,C and 2B). A single branch from the musculocutaneous nerve may bifurcate to supply the long and short heads (twothirds of specimens; Fig. 2A) or the nerves for each head may arise as two nerves directly from the musculocutaneotis nerve (one-third of specimens: Fig. 1A). These nerves then each divide into branches which supply each of the compartments (Figs. 1A and 2A). Higher order branches to fascicles within each compartment are also found, suggesting that a c o m p a r t m e n t could contain smaller subunits (Figs. 1A and 2A). In other words, the compartment may not be the smallest functional unit (although the data of ter H a a r Romeny [7, 8] suggest they are the smallest unit). Such higher order branching is more common in the short head (Fig. IA). The branches do n o t always end at the mid-point of the muscle belly. Often there arc branches directed towards the proximal or distal (less often) portion of the long and short heads (Fig. 1A). These variations are more c o m m o n in the long head (Fig. 1A). The biceps brachii is clearly a muscle that has anatomical neuromuscular compartments. The long and short heads receive separate nerve branches from the musculocutaneous nerve, each has separate origins from the scapula, and each attaches differently to the tendon of insertion. There are, however, smaller compartments than those defined as the long and short heads. These compartments within the long and short heads are delined by muscle architecture and the nerve branching pattern. Both heads have architectural compartments that are innervated by private branches from the main muscle nerves and which have distinct attachments to the lendon of insertion. Moreover, the architectural and nerve branching pattern compartments are congruent. The result is that each head of the biceps brachii is divide& at least grossly, into medial to lateral in-parallel neuromuscular compartments. The apparent aggregation of m o t o r unit territories described by ter Haar Romeny et al. [7, 8] is strikingly similar to the in-parallel organization of neuromuscular compartments observed in the present study. If this congruence is substantiated by future studies, then the nolion that neuromuscular compartments represent elements in the design of skeletal muscles, as first proposed by English and Letbetter [6] for cat ankle extensor muscles, can be extended to the human biceps brachii muscle.
In addition, the present findings of apparent in-parallel neuromuscular compartments is true not only for the long head, but also for the short head. The medial to lateral organization of the neuromuscular compartments is also consistent with results of previous studies [1,2, 10] that examined the innervation zones of the biceps. In these studies [1, 2, 101 the innervation zones were in a strip running medial to lateral midway between the origin and insertion of the biceps. The present study also demonstrates that, except for occasionally seen recurrent and distal branches, most muscle nerves end approximately midway between origin and insertion of the biceps. Future studies will have to determine whether these recurrent and distal branches are motor nerves to muscle or are, for example~ afferents from Golgi tendon organs or muscle spindles. Future studies will also have to address whether the anatomical compartments (this study) and functional compartments (ter H a a r Romeny et al. [7, 8]) serve a mechanical purpose. This issue can be addressed by correlating E M G activity from the compartments with mechanical measurements. The differences between the attachments of the compartments suggest the possibility of mechanical differences between compartments. Moreover, the fact that the short-head appears to contribute more to the bicipital aponeurosis also supports the notion of mechanical differences between the long and short heads, and possibly their neuromuscular compartments. Indeed, evidence from Buchanan et al. [3] suggests that the long head is capable of generating force in more directions than the short head. The author thanks the American Paralysis Association for partial funding of the study: Lance Cherry for work during the early phases of the study: Lisa Walker for assistance in the preparation of early drafts of the manuscript, Dr. Arthur English and Patsy Bryan for assistance with the figures, and also thanks to Dr. English and Dr. Steven Wolf for comments on the manuscript. 1 Aquilonius, S.-M., Askmark, H., Gillberg, P.-G., Nandedkar, S., Olsson, Y. and Stalberg, E., Topographical localization of motor endplates in cryosections of whole human muscles, Muscle Nerve, 7 (1984) 287 293. 2 Askmark, H., Gillberg, P,-K. and Aquilonius, S.-M., Autoradiographic visualization of extrajunctional acctylcholinereceptors in whole human biceps brachii muscle: changes in amyotrophic lateral sclerosis, Acta Neurol. Scand., 72 (1985) 344 347. 3 Buchanan. T.S., Almdale, D.P.J.. Lewis. J.L. and Rymer, W,Z., Characteristics of synergic relations during isometric contractions of human elbow muscles, J. Neurophysiol., 56 (1986) 1225 1241. 4 Chanaud, C.M.. Pratt, C.A. and Loeb. G.E., Functionally complex muscles of the cat hindlimb. V. The roles of histochemical fiber-type regionalization and mechanical heterogeneity in differential muscle activation, Exp. Brain Res.. 85 ( 1991 ) 300 313.
102 5 English, A.W., An electromyographic analysis of compartments in cat lateral gastrocnemius muscle during unrestrained locomotion, J. Neurophysiol., 52 (1984) 114 125. 6 English, A.W. and Letbetter, W.D., Anatomy and innervation patterns of cat lateral gastrocnemius and plantaris muscles, Am. J. Anat.. 164 (1982) 67- 77. 7 ter Haar Romeny, B.M., Denier van der Gon, J.J. and Gielen, C.C.A.M., Relation between location of a motor unit in the human biceps brachii and its critical firing levels for different, tasks. Exp. Neurol., 85 (9814) 631 650. 8 ter Haar Romeny. B.M., Denier van der Gon, J.J. and Gielen, C,C.A.M., Changes in recruitment order of motor units in the human biceps muscle, Exp. Neurol.. 78 (1982) 360-368. 9 Letbetter, W.D., Influence of intramuscular nerve branching on motor unit organization in medial gastrocnemius muscle, Anat. Rec., 178 (1974) 402. 10 Masuda, T., Miyano, H and Sadoyama, T., The position of innervation zones in the biceps brachii investigated by surface electromyography, I.E.EE. Trans B.M.E., 32 (1985) 3642. 11 McMahon, T., Pianta, T., Couch, L., Wolf, S., Segal, R., Mason. L., Craft, T., English, A. and Catlin, R, Normalized electromyographic activity patterns in human extensor carpi radialis longus and flexor carpi radialis muscles: Differential activity. In P.A. Ander-
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soil, D.J. Hobart and J.V. Danoff(Eds.), Elecmnnyographical Kinesiology: Proceedings of the 8th Congress of the hucrnatiomd Society of Electrophysiological Kinesiology. Elsevier. Amsterdam. 1991, pp. 39-42. Richardson-Bond, C., Coratti. L., Mast. A., Wolf, S., Catlin, P. Segal, R. and English, A., Patterns ot'electromyographic activity m the human lateral gastrocnemius muscle during weightbearing and mm-weightbearing tasks. In P.A. Anderson, D.J. Hobart and J.V. Danoff (Eds.), Electromyographical Kinesiology: Proceedings of the 8th Congress of the International Society of Electrophysiological Kinesiology, Elsevier, Amsterdam, 1991. pp. 65 68. Segal, R.L., Wolf, S.L., DeCamp, M.J., Chopp, M.T. and English, A.W., Anatomical partitioning of three multiarticular human muscles, Acta Anat., 142 (1991) 261 266. Windhorst, U., Hamm, T.M. and Stuart, D.G.. On the function of muscle and reflex partitioning, Behav. Brain Sci., 12 (1989) 629 681. van Zuylen, E.J., Gielen, C.C.A.M. and Denier van der Gon, J.J., Coordination and inhomogeneous activation of human arm muscles during isometric torques..1. Neurophysiol., 60 (1988) 1523 1548.
Neuromuscular compartments in the human biceps brachii muscle R i c h a r d L. Segal Division q[Ph.vsical Therapy, Department of Rehabilitation Medicine. and Department o]Anatomy and Cell Biology, Emor~ University School q[' Medicine, Atlanta, GA 30322 ( USA ) (Received 15 January 1992; Revised version received 10 March t992; Accepted 11 March 1992)
Key wordsv Biceps brachii; Human; Neuromuscular; Compartment; Architecture; lnnervation; Anatomy Electrophysiological evidence suggests that the human biceps brachii muscle is organized into functional neuromuscular compartments. The purpose of this study was to determine whether there was an anatomical basis for these compartments. Dissection of the biceps revealed both architectural and nerve branching pattern compartmentalization within the muscle. Although the biceps brachii is grossly subdivided into long and short heads, these heads are further subdivided into roughly parallel architectural compartments. Moreover, these architectural compartments usually receive a private nerve branch, thus supporting the notion that the human biceps brachii has neuromuscular compartments.
The identification of the peripheral elements controlled by the central nervous system (CNS) to generate movement is controversial. Questions exist regarding the smallest functional elements (e.g. motor units, neuromuscular compartments) controlled by the CNS. Resuits from studies by Letbetter and English [6, 9] demonstrated that the cat lateral gastrocnemius muscle is organized into neuromuscular compartments. Moreover, these compartments can behave differently according to task requirements [5]. Thus, these neuromuscular compartments may be the smallest component controlled by the CNS. For a global perspective of the issue of neuromuscular compartments within muscles refer to the eloquent review by Windhorst et al. [14]. In addition, the terminology used to describe neuromuscular compartments is confusing. This issue is addressed comprehensively by Chanaud et al, [4]. For the purposes of this paper, the term neuromuscular compartment will be used to describe muscle subunits delineated by architecture and nerve branching patterns. Recent investigations from this laboratory have examined anatomical and functional neuromuscular compartments in three human muscles: lateral gastrocnemius (LG), flexor carpi radialis (FCR), and extensor carpi radialis longus (ECRL) [11--13]. Other laboratories studying compartments in human muscle have focused only C))rre,spondence." R.L. Segal, Room 209, Center tbr Rehabilitation Medicine, Emory University School of Medicine, 1441 Clifton Road, NE, Atlanta, GA 30322, USA.
on electromyographic (EMG) recordings and have provided no anatomical basis for their choice of recording sites. Electrophysiological studies by ter Haar Romeny et al. [7, 8] and van Zuyten et al. [15] have demonstrated a topographical organization of the long head of the human biceps brachii that is related to the critical motor unit firing levels for different tasks. Thus, within the long head of the biceps brachii, motor units recorded from lateral locations were recruited for elbow flexion, units recorded from medial sites were recruited for supination or linear combinations of flexion and supination; and more centrally located units were recruited for non-linear combinations of flexion and supination. There is no evidence in the literature to suggest that the human biceps brachii is anatomically organized in a manner that would provide a basis for the results of ter Haar Romeny et al. [7, 8] and van Zuylen et al. [15]. Studies reporting the staining of the biceps brachii using either acetylcholinesterase histochemistry [1] or the binding of [3H]~-bungarotoxin [2] have shown that endplates lie along a strip in the middle of the bellies from medial to lateral, a region whose extent is 5--10 mm from proximal to distal. Surface EMG studies used to map innervation zones also indicate that the motor end-plates lie in a row midway between the proximal and distal bony attachments of the muscle [10]. These studies, however, did not investigate the branching patterns of muscle nerves or the gross architecture of the muscle. Thus, whether the end-plate organization reflects an organization that supports the physiological data of ter Haar
99
B
C
Fig. 1. Photographs of biceps brachii specimens. A: a deep or posterior view of a biceps specimen. The coracobrachialis is attaching proximally with the short head {labeled by number 1). The neuromuscular compartments are clearly visible from this view. In this specimen the nerve branches Io the long (labeled by number 2) and short heads come off directly from the musculocutaneous nerve. Also, notice the crus of the tendon of insertion ~ hich is labeled as number 3. In this photograph left is distal and the top is medial. B: the superficial or anterior view of the same spccimen as in A. Notice th~tt neuromuscular compartments are Hol visible from this view. The superficial view shows how the long head (labeled as number 2) inserts more proximally ~mto the tcndon of insertion (labeled as number I ) than does the short head. In lhis photograph left is distal, the top is latcral and the short head is labeled by number 3. (7: a superficial or anterior vicw of the distal end of another specimen with the samc orientation as B. This photograph shows the more proximal attachment of the long head (labeled by number 3) onto tendon of insertion (labeled as number I). The photograph also shows the short hcnd (labclcd by number 4) attaching more intimately to the bicipital aponeurosis {labeled by number 2) than the long h e a d Both the long and short heads attach to the tendon proper (labeled by number 1}.
Romeny and coworkers [7, 8] remains unknown. The nerve branching patterns, muscle architecture, and their relationship may provide an anatomical basis for the physiological findings [7, 8] of functional neuromuscular compartments in human biceps brachii. Thus, the present work was undertaken to examine whether there is morphological evidence for neuromuscular compart-
ments within the human biceps brachii, particularly its long head. Samples of biceps brachii ( n = 6 : 3 right: 3 left) were obtained from perfused human cadavers donated to the Medical School's Department of Anatomy and Cell Biology. The average age at death was 72 years. Blunt dissection was conducted with the aid of a visor-mounted mag-
I00
nifier (5x) or a dissecting microscope (10-40x) on muscles both in situ and after removal from the cadavers. The courses taken by branches of the musculocutaneous nerve to each muscle and their branches to each head were defined and compared between cadavers to evaluate their consistency. The major branches of each of the nerves were followed as they divided within the muscle until they could no longer be followed at 10-40x. The orientation of the tendons of origin and insertion, and the direction of muscle fibers were also noted while performing the dissection. The muscle fiber direction and points of attachment along with nerve branch relationships were then documented with sketches, photographs and written descriptions. The angles of pennation were not measured in the present study. Muscle fibers were carefully removed as necessary to view the full extent of their tendinous attachments. The drawings in the text reflect typical patterns of architecture and innervation of these muscles. The biceps brachii has long (lateral) and short (medial) heads, The tendons of origin for both heads become broad as they course from proximal to distal and do not end until about the juncture of the proximal one-third and middle one-third of each head, respectively. Muscle
fibers take origin from the deep suri;ace of these broad tendons (Fig. IA). The muscle fibers in both heads arc arranged in parallel along the longitudinal axis of lhc muscle (Figs. 1 and 2). However, there are fl'om two to four natural groupings of the fibers in each head when viewed from the deep surface (Figs. I A and 2A). These groupings will be referred to as the architectural portion of the neuromuscular compartment. The fiber groupmgs are n o t clearly visible from the anterior or superficial view (Figs. IB and 2B). Thus, because most observers only view the superficial portion of the biceps, the presence of the neuromuscular compartments has not previously been documented. The two heads of the biceps 'fuse' just proximal(Figs. 1B and 2B) to the elbow joint, attaching distally to the radial tuberosity of the forearm via the biceps tendon and to the ulna via the bicipital aponeurosis (Figs. lC and 2B: laceratus fibrosis). The lateral compartment of the long head and the medial compartment of the short head attach more distally onto the deep surface of the tendon of insertion (Fig. 2A). The medial compartment of the long head and the lateral compartment of the short head attach more proximally and superficially onto the tendon of insertion (Fig. 2A). In addition, these muscle
B. Anterior or Superficial Surface
A. Posterior or Deep Surface )roximal
-- Short head
nerve
Long head
Branch to long head
head Medial
Lateral Lateral Medial head Short
Crus
Tendon
Tendon of insertion
Distal
aponeurosis Distal
Fig. 2. Drawings of biceps brachii muscle. A: a view of the deep or posterior surface of the biceps. The asterisks demarcate neuromuscular compartments of the long and short heads. The main nerves to the long and short heads do n o t come directly from the musculocutaneous nerve in two-thirds of the specimens, but from the bifurcation of a branch of the musculocutaneous nerve (compare to Fig. IA). Notice that there are usually private nerve branches to the compartment. B: a superficial or anterior view of biceps. The neuromuscular compartments are n o t visible from this view. Notice that the long head inserts more proximally than the short head. The short head is more closely associated with the bicipital aponeurosis which attaches to the ulna.
101 fibers attach along a crus of the tendon of insertion (Figs. 1A and 2A). The fibers from the short head are more intimately linked to the bicipital aponeurosis than fibers from the long head (Fig. 1C). However, the long head does link to the aponeurosis (Fig. 1C). Finally the fibers from the long head attach more proximally to the anterior surface of the tendon of insertion than those from the short head (Figs. 1B,C and 2B). A single branch from the musculocutaneous nerve may bifurcate to supply the long and short heads (twothirds of specimens; Fig. 2A) or the nerves for each head may arise as two nerves directly from the musculocutaneotis nerve (one-third of specimens: Fig. 1A). These nerves then each divide into branches which supply each of the compartments (Figs. 1A and 2A). Higher order branches to fascicles within each compartment are also found, suggesting that a c o m p a r t m e n t could contain smaller subunits (Figs. 1A and 2A). In other words, the compartment may not be the smallest functional unit (although the data of ter H a a r Romeny [7, 8] suggest they are the smallest unit). Such higher order branching is more common in the short head (Fig. IA). The branches do n o t always end at the mid-point of the muscle belly. Often there arc branches directed towards the proximal or distal (less often) portion of the long and short heads (Fig. 1A). These variations are more c o m m o n in the long head (Fig. 1A). The biceps brachii is clearly a muscle that has anatomical neuromuscular compartments. The long and short heads receive separate nerve branches from the musculocutaneous nerve, each has separate origins from the scapula, and each attaches differently to the tendon of insertion. There are, however, smaller compartments than those defined as the long and short heads. These compartments within the long and short heads are delined by muscle architecture and the nerve branching pattern. Both heads have architectural compartments that are innervated by private branches from the main muscle nerves and which have distinct attachments to the lendon of insertion. Moreover, the architectural and nerve branching pattern compartments are congruent. The result is that each head of the biceps brachii is divide& at least grossly, into medial to lateral in-parallel neuromuscular compartments. The apparent aggregation of m o t o r unit territories described by ter Haar Romeny et al. [7, 8] is strikingly similar to the in-parallel organization of neuromuscular compartments observed in the present study. If this congruence is substantiated by future studies, then the nolion that neuromuscular compartments represent elements in the design of skeletal muscles, as first proposed by English and Letbetter [6] for cat ankle extensor muscles, can be extended to the human biceps brachii muscle.
In addition, the present findings of apparent in-parallel neuromuscular compartments is true not only for the long head, but also for the short head. The medial to lateral organization of the neuromuscular compartments is also consistent with results of previous studies [1,2, 10] that examined the innervation zones of the biceps. In these studies [1, 2, 101 the innervation zones were in a strip running medial to lateral midway between the origin and insertion of the biceps. The present study also demonstrates that, except for occasionally seen recurrent and distal branches, most muscle nerves end approximately midway between origin and insertion of the biceps. Future studies will have to determine whether these recurrent and distal branches are motor nerves to muscle or are, for example~ afferents from Golgi tendon organs or muscle spindles. Future studies will also have to address whether the anatomical compartments (this study) and functional compartments (ter H a a r Romeny et al. [7, 8]) serve a mechanical purpose. This issue can be addressed by correlating E M G activity from the compartments with mechanical measurements. The differences between the attachments of the compartments suggest the possibility of mechanical differences between compartments. Moreover, the fact that the short-head appears to contribute more to the bicipital aponeurosis also supports the notion of mechanical differences between the long and short heads, and possibly their neuromuscular compartments. Indeed, evidence from Buchanan et al. [3] suggests that the long head is capable of generating force in more directions than the short head. The author thanks the American Paralysis Association for partial funding of the study: Lance Cherry for work during the early phases of the study: Lisa Walker for assistance in the preparation of early drafts of the manuscript, Dr. Arthur English and Patsy Bryan for assistance with the figures, and also thanks to Dr. English and Dr. Steven Wolf for comments on the manuscript. 1 Aquilonius, S.-M., Askmark, H., Gillberg, P.-G., Nandedkar, S., Olsson, Y. and Stalberg, E., Topographical localization of motor endplates in cryosections of whole human muscles, Muscle Nerve, 7 (1984) 287 293. 2 Askmark, H., Gillberg, P,-K. and Aquilonius, S.-M., Autoradiographic visualization of extrajunctional acctylcholinereceptors in whole human biceps brachii muscle: changes in amyotrophic lateral sclerosis, Acta Neurol. Scand., 72 (1985) 344 347. 3 Buchanan. T.S., Almdale, D.P.J.. Lewis. J.L. and Rymer, W,Z., Characteristics of synergic relations during isometric contractions of human elbow muscles, J. Neurophysiol., 56 (1986) 1225 1241. 4 Chanaud, C.M.. Pratt, C.A. and Loeb. G.E., Functionally complex muscles of the cat hindlimb. V. The roles of histochemical fiber-type regionalization and mechanical heterogeneity in differential muscle activation, Exp. Brain Res.. 85 ( 1991 ) 300 313.
102 5 English, A.W., An electromyographic analysis of compartments in cat lateral gastrocnemius muscle during unrestrained locomotion, J. Neurophysiol., 52 (1984) 114 125. 6 English, A.W. and Letbetter, W.D., Anatomy and innervation patterns of cat lateral gastrocnemius and plantaris muscles, Am. J. Anat.. 164 (1982) 67- 77. 7 ter Haar Romeny, B.M., Denier van der Gon, J.J. and Gielen, C.C.A.M., Relation between location of a motor unit in the human biceps brachii and its critical firing levels for different, tasks. Exp. Neurol., 85 (9814) 631 650. 8 ter Haar Romeny. B.M., Denier van der Gon, J.J. and Gielen, C,C.A.M., Changes in recruitment order of motor units in the human biceps muscle, Exp. Neurol.. 78 (1982) 360-368. 9 Letbetter, W.D., Influence of intramuscular nerve branching on motor unit organization in medial gastrocnemius muscle, Anat. Rec., 178 (1974) 402. 10 Masuda, T., Miyano, H and Sadoyama, T., The position of innervation zones in the biceps brachii investigated by surface electromyography, I.E.EE. Trans B.M.E., 32 (1985) 3642. 11 McMahon, T., Pianta, T., Couch, L., Wolf, S., Segal, R., Mason. L., Craft, T., English, A. and Catlin, R, Normalized electromyographic activity patterns in human extensor carpi radialis longus and flexor carpi radialis muscles: Differential activity. In P.A. Ander-
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soil, D.J. Hobart and J.V. Danoff(Eds.), Elecmnnyographical Kinesiology: Proceedings of the 8th Congress of the hucrnatiomd Society of Electrophysiological Kinesiology. Elsevier. Amsterdam. 1991, pp. 39-42. Richardson-Bond, C., Coratti. L., Mast. A., Wolf, S., Catlin, P. Segal, R. and English, A., Patterns ot'electromyographic activity m the human lateral gastrocnemius muscle during weightbearing and mm-weightbearing tasks. In P.A. Anderson, D.J. Hobart and J.V. Danoff (Eds.), Electromyographical Kinesiology: Proceedings of the 8th Congress of the International Society of Electrophysiological Kinesiology, Elsevier, Amsterdam, 1991. pp. 65 68. Segal, R.L., Wolf, S.L., DeCamp, M.J., Chopp, M.T. and English, A.W., Anatomical partitioning of three multiarticular human muscles, Acta Anat., 142 (1991) 261 266. Windhorst, U., Hamm, T.M. and Stuart, D.G.. On the function of muscle and reflex partitioning, Behav. Brain Sci., 12 (1989) 629 681. van Zuylen, E.J., Gielen, C.C.A.M. and Denier van der Gon, J.J., Coordination and inhomogeneous activation of human arm muscles during isometric torques..1. Neurophysiol., 60 (1988) 1523 1548.
