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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 con-
trolled by the central nervous system (CNS) to generate
movement is controversial. Questions exist regarding the
smallest functional elements (e.g. motor units, neu-
romuscular compartments) controlled by the CNS. Re-
suits from studies by Letbetter and English [6, 9] demon-
strated that the cat lateral gastrocnemius muscle is or-
ganized into neuromuscular compartments. Moreover,
these compartments can behave differently according to
task requirements [5]. Thus, these neuromuscular com-
partments may be the smallest component controlled by
the CNS. For a global perspective of the issue of neu-
romuscular compartments within muscles refer to the el-
oquent review by Windhorst et al. [14]. In addition, the
terminology used to describe neuromuscular compart-
ments is confusing. This issue is addressed comprehen-
sively by Chanaud et al, [4]. For the purposes of this
paper, the term neuromuscular compartment will be
used to describe muscle subunits delineated by architec-
ture and nerve branching patterns.
Recent investigations from this laboratory have exam-
ined anatomical and functional neuromuscular compart-
ments in three human muscles: lateral gastrocnemius
(LG), flexor carpi radialis (FCR), and extensor carpi ra-
dialis longus (ECRL) [11--13]. Other laboratories study-
ing 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 pro-
vided 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 evi-
dence 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 end-
plates 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, how-
ever, did not investigate the branching patterns of muscle
nerves or the gross architecture of the muscle. Thus,
whether the end-plate organization reflects an organiza-
tion 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 pres-
ent 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 Biol-
ogy. The average age at death was 72 years. Blunt dissec-
tion was conducted with the aid of a visor-mounted mag-
I00

nifier (5x) or a dissecting microscope (10-40x) on mus-
cles 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 evalu-
ate 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 per-
forming the dissection. The muscle fiber direction and
points of attachment along with nerve branch relation-
ships 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 pres-
ence of the neuromuscular compartments has not previ-
ously 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

A. Posterior or Deep Surface B. Anterior or Superficial Surface

)roximal

-- Short head
nerve

Long head

Branch to long
head

head
Medial
Lateral
Lateral
Medial

head
Short

Crus Tendon

Tendon of insertion aponeurosis

Distal 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.

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 ante-
rior 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 (two-
thirds of specimens; Fig. 2A) or the nerves for each head
may arise as two nerves directly from the musculocutane-
otis 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, sug-
gesting that a c o m p a r t m e n t could contain smaller sub-
units (Figs. 1A and 2A). In other words, the compart-
ment 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 com-
mon 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 dis-
tal (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 anatom-
ical neuromuscular compartments. The long and short
heads receive separate nerve branches from the musculo-
cutaneous 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 de-
lined 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 di-
vide& at least grossly, into medial to lateral in-parallel
neuromuscular compartments.
The apparent aggregation of m o t o r unit territories de-
scribed by ter Haar Romeny et al. [7, 8] is strikingly sim-
ilar to the in-parallel organization of neuromuscular
compartments observed in the present study. If this con-
gruence is substantiated by future studies, then the no-
lion that neuromuscular compartments represent ele-
ments in the design of skeletal muscles, as first proposed
by English and Letbetter [6] for cat ankle extensor mus-
cles, can be extended to the human biceps brachii muscle.
101
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 neuromuscu-
lar compartments is also consistent with results of previ-
ous 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 pres-
ent 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 cor-
relating E M G activity from the compartments with me-
chanical measurements. The differences between the at-
tachments of the compartments suggest the possibility of
mechanical differences between compartments. Moreo-
ver, the fact that the short-head appears to contribute
more to the bicipital aponeurosis also supports the no-
tion of mechanical differences between the long and
short heads, and possibly their neuromuscular compart-
ments. Indeed, evidence from Buchanan et al. [3] sug-
gests 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 manu-
script, 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., Autoradi-
ographic 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 pat-
terns 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 inner-
vation zones in the biceps brachii investigated by surface electro-
myography, 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 electromyogra-
phic activity patterns in human extensor carpi radialis longus and
flexor carpi radialis muscles: Differential activity. In P.A. Ander-
soil, D.J. Hobart and J.V. Danoff(Eds.), Elecmnnyographical Ki-
nesiology: Proceedings of the 8th Congress of the hucrnatiomd So-
ciety of Electrophysiological Kinesiology. Elsevier. Amsterdam.
1991, pp. 39-42.
12 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 Electrophysiologi-
cal Kinesiology, Elsevier, Amsterdam, 1991. pp. 65 68.
13 Segal, R.L., Wolf, S.L., DeCamp, M.J., Chopp, M.T. and English,
A.W., Anatomical partitioning of three multiarticular human mus-
cles, Acta Anat., 142 (1991) 261 266.
14 Windhorst, U., Hamm, T.M. and Stuart, D.G.. On the function of
muscle and reflex partitioning, Behav. Brain Sci., 12 (1989) 629
681.
15 van Zuylen, E.J., Gielen, C.C.A.M. and Denier van der Gon, J.J.,
Coordination and inhomogeneous activation of human arm mus-
cles during isometric torques..1. Neurophysiol., 60 (1988) 1523
1548.