Does the Nerve Supply to Both the Superficial and Deep Surfaces of Pectoralis Major Imply Two Separate Developmental Origins?

J. Anat. (1996) 188, pp. 263-268, with 4 figures Printed in Great Britain 263

Does the nerve supply to both the superficial and deep surfaces of pectoralis major imply two separate developmental origins?

HARUMICHI SHINOHARA Division of Human Sciences, Faculty of Medicine, Toyama Medical and Pharmaceutical University, Toyama, Japan

(Accepted 23 July 1995)

ABSTRACT The nature of the nerve supply to the 'pocket' of pectoralis major was examined on 7 randomly selected sides of 5 embalmed cadavers. The pocket was a U-shaped muscular fold, opening cranially. The anterior limb and inner surface of the fold were supplied by nerve branches that originated from the middle segment of the pectoral nerve loop and penetrated pectoralis minor. The outer surface of the posterior limb was supplied by one or two branches that extended from the caudal segment of the pectoral nerve loop. If the muscular U-shaped fold is unfolded, it becomes obvious that the posterior wall of the pocket forms the most caudal part of pectoralis major and is supplied from both the superficial (anterior) and deep (posterior) surfaces. This dual surface supply does not suggest any aspect of the developmental origin of the pocket but may simply be due to the relative positions of the pectoralis major and its nerve.

Key words: Skeletal muscle; pectoralis major; dual innervation. the force for inspiration (Basmajian, 1980). However, INTRODUCTION Sato (1973) & Yamada (1987) questioned this putative The 'law' of fusion is one of the logical extensions of homology on the basis ofnerve supply. The intercostal a classic tenet in anatomy, namely that a nerve reaches nerves supply the external abdominal oblique from its target muscle early in development (see Shinohara, the superficial surface in the cranial part of the muscle 1995). According to this law, when a muscle is and from the deep surface in its caudal part. By supplied by two different nerves, the muscle is thought contrast, the entire external intercostal is supplied by to have been formed by the fusion of two muscle the intercostal nerves from the muscle's deep surface. primordia, each of which had been supplied in- Sato (1973) speculated, on the basis of this difference dependently by one of the two nerves. Furthermore, in nerve supply and the comparative anatomy of the when a muscle is supplied both from the superficial trunk musculature (Ouchi, 1987), that the external and deep surfaces, the muscle is considered to have abdominal oblique is derived from a muscle anlage been formed by the fusion of two different muscle termed the ventral oblique and is not homologous primordia, each ofwhich was originally supplied from with the external intercostal which is derived from an opposite directions. Thus some gross anatomists have anlage referred to as the dorsal oblique. placed considerable emphasis on whether a muscle is Pectoralis major is known to be divided into several supplied from the superficial or deep surfaces or from portions and is supplied by the medial and lateral both. It is considered that this may provide clues as to pectoral nerves (Williams et al. 1989), but the pattern the developmental origin of the muscle and homology of innervation to the different portions is imperfectly with other muscles. A good example is the external understood. The present study provides a neuro- abdominal oblique muscle. This muscle is regarded as anatomical complement to the study by Ashley (1952) a morphological and functional homologue of the in which the muscle bundle arrangement of pectoralis external intercostals: the fibres of both muscles run major was clarified. During an analysis of the nerve downwards and forwards, and both muscles provide distribution, the present author realised that pectoralis Correspondence to Dr Harumichi Shinohara, Division of Human Sciences, Faculty of Medicine, Toyama Medical and Pharmaceutical University, Sugitani 2630, Toyama 930-01, Japan. 264 H. Shinohara

Fig. 1. Anterior (superficial) surface ofpectoralis major. The muscle consists ofclavicular (C), sternocostal (SC) and abdominal (A) portions. Note that the abdominal portion and part of the sternocostal portion twist to form the conjoined tendon of insertion. Nerve supply to pectoralis major 265 major is an example of a muscle with a dual mode of sternocostal and abdominal portions joined and innervation. converged to a common tendon of insertion, which was approximately 6 cm in craniocaudal length and MATERIALS AND METHODS attached to the crest of the greater tuberosity (Figs 1, 2). The conjoined tendon twisted and formed a The pectoral muscles and their nerve supply were 'pocket' that opened cranially (Zuckerkandl, 1910; examined on 5 randomly selected sides of 4 male Eisler, 1912). To a rough approximation, the anterior cadavers and both sides of 1 female cadaver. Their wall of the pocket was formed by the sternocostal from 56 to 93 ages ranged y. portion and the lower (caudal) margin by the The skin to the subcutaneous tissue was attached abdominal portion. The posterior wall was formed removed extensively from the cervical, anterior thor- partly by the abdominal portion and mostly by a acic and abdominal, and proximal humeral regions. muscular slip that extended from the 6th and 7th The entire superficial surface of pectoralis major was costal cartilages. The muscular slip is referred to as the exposed, and the muscle was cut at its origins and 'deep' layer of the sternocostal portion and was to the humeral insertion. The deep surface of inverted distinguishable from the 'superficial' layer of the superficial surface of pectoralis the muscle and the sternocostal portion that formed the anterior wall of minor were cleaned. The costal origin of pectoralis the pocket. The pocket was closed medially by the minor was cut and inverted to its coracoid insertion. exchange of numerous muscle fascicles between the attention was paid to preserving the nerves Special superficial and deep layers of the sternocostal portion. distributed to the two pectoral muscles. The nerves It was also closed laterally by fusion of the tendons of were followed proximally to the loop formed by the the anterior and posterior walls; the pocket was thus lateral and medial pectoral nerves. several centimetres in length (Figs 2, 3). It was In addition, microdissection under a stereoscopic noteworthy that the surface of the inside wall of the microscope was performed to ascertain whether the pocket (Figs 3, 4a) was continuous with and thus part nerves to the muscles include components of pectoral of the deep surface (Figs 3, 4b) of pectoralis major. the lateral and medial pectoral nerves and to both Similarly, the surface of the outside wall of the pocket clarify the intramuscular distribution of these nerves (Fig. 4a, large asterisk) was part of the superficial in the caudal of pectoralis major. part surface (Fig. 4b, large asterisk) of the muscle. Pectoralis major was supplied by the lateral and RESULTS medial pectoral nerves (Figs 2, 3, 4a). The 2 nerves Pectoralis major was divisible into 3 portions, namely formed a (pectoral) loop over the axillary artery, and clavicular, sternocostal and abdominal, according to several branches extended from the pectoral loop. their origin. The clavicular portion arose from the These branches could be divided into 3 groups, medial half of the clavicle and was inserted into the namely, the cranial, middle and caudal groups, crest of the greater tuberosity of the humerus. This depending on their origin. The cranial branches portion was most superficially located, and its entire originated from near the lateral pectoral nerve, the surface was visible in an anterior view of the muscle middle branches from the midportion between the (Fig. 1). The sternocostal portion originated widely lateral and medial pectoral nerves, and the caudal from the sternum and upper 7 costal cartilages and branches from near the medial pectoral nerve. The ribs, and it accounted for the major part of the muscle. cranial branches supplied the clavicular portion and The abdominal portion arose from the rectus sheath, the cranial half of the sternocostal portion. The but its fibres were not clearly distinguishable from middle branches supplied pectoralis minor, penetrated those of the external abdominal oblique. Moreover, the muscle, and further supplied the caudal half of the muscle fibres of this portion arose from the costal pectoralis major. One or two of the middle branches cartilages and ribs; the border between these fibres reached and supplied the cranial margin and the and those of the sternocostal portion was indefinite. inside surface of the pocket. There was at least one Thus the abdominal portion of pectoralis major was, caudal branch. This branch consistently reached as far strictly speaking, only a thin muscular slip. The as the outside surface of the posterior wall of the

Fig. 2. Posterior (deep) surface of pectoralis major. The pectoral pocket opens cranially (broken line and broken arrows). Its posterior wall (large asterisk) is formed mostly by the deep layer of the sternocostal portion (small asterisks) and partly by the abdominal portion (A). The lateral (L) and medial (M) pectoral nerves form a loop that sends off several branches. These branches are usually divided into three groups: the cranial branches (1, 2), middle branches (3, 4) and caudal branches (5). The nerves supplying the interior of the pectoral pocket are indicated by arrowheads. Pm, pectoralis minor muscle. 266 H. Shinohara

Fig. 3. The pectoral pocket in the same specimen as in Figure 2 has been opened widely. Pectoralis minor was inverted so as to correspond with the nerves seen in Figure 2. Note that the nerve twigs extending from the middle branch supply the interior of the pectoral pocket (arrowheads). Abbreviations as in Figure. 2.

Lb_PM L >;PM

4a 4b Fig. 4. Schematic illustrations of pectoralis major (PM) and its nerve supply. The nerves numbered 1-5 and the large asterisks correspond to those in Figures 2 and 3. Note that the posterior wall of the pocket is supplied both from the superficial and deep surfaces. This point becomes more obvious if the pocket wall is unfolded (b). The small asterisks indicate the inside of the pocket. Abbreviations as in Figure. 2. pocket. There were minor variations; for example, fundamental pattern of innervation described above extra twigs from the cranial branches might invade the was very stable and is presented schematically in territory of the middle branches. However, the Figure 4a. Nerve supply to pectoralis major 267

Fine dissection of the nerves revealed that all with the conclusions derived from comparative anat- branches arising from the pectoral nerve loop con- omy. Lewis stated that pectoralis major and minor are tained components of both the lateral and medial derived from a common premuscle mass in the lower pectoral nerves. There was a tendency for the branch cervical region. This muscle mass becomes flattened that originated closer to the lateral pectoral nerve to and splits into the future pectoral muscles during its receive a thicker fascicle from the lateral pectoral caudoventral extension, and muscle bundles of nerve and a thinner fascicle from the medial pectoral pectoralis major begin to overlap at the insertion to nerve. Similarly, the branch originating closer to the generate the adult form. Of particular importance is medial pectoral nerve received a thicker fascicle from his observation that the tendon of insertion of the medial pectoral nerve and a thinner fascicle from pectoralis major consists initially of a single sheet, but the lateral pectoral nerve. The nerve branches to the later the second deeper sheet spreads proximally from posterior wall of the pocket did not communicate the distal end of the first layer. In a 40 mm embryo, within the muscle. They were distributed in inde- the second sheet exceeds the superficial sheet in pendent and mutually complementary regions (Fig. breadth. Clearly, he observed that the formation of 4a). the pocket had occurred by 'spreading' from the pre- existing muscle and not by 'fusion' of two muscle primordia. DISCUSSION The classic tenets regarding nerve-muscle speci- Pectoralis major is not a simple plate muscle but has ficity are invalid in the light of present knowledge a fold or pocket (Fig. 4a). If this is unfolded, it (Straus, 1946; Shinohara, 1996). Therefore, specu- becomes obvious that the posterior wall of the pocket, lations as to the origin and development of a muscle namely, the most caudal part of pectoralis major, based on its nerve supply are also invalid. The receives its nerve supply both from the superficial and pectoral nerve extends from a deep location and deep surfaces (Fig. 4b). Should the dual surface reaches the deep surface of pectoralis major and its supply to the pocket of pectoralis major therefore be pocket, with a resultant dual surface supply. The interpreted as evidence that the part developed from nerve supply to the pectoral pocket is an example of two different muscle primordia? Some authors have the phenomenon whereby a dual surface supply can already answered this question in the affirmative from occur irrespective of the developmental origin of a the perspective ofcomparative anatomy. Zuckerkandl muscle. 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