Innervation of the Superficial Flexor Muscles of the Lower Leg of the Formosan Monkey : With Special Reference to the Medial Sural Cutaneous Nerve

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1 Oka iimas Folia Anat. Jpn., 57(2-3) : , August 1980 Innervation of the Superficial Flexor Muscles of the Lower Leg of the Formosan Monkey : With Special Reference to the Medial Sural Cutaneous Nerve By SEIJI NAGASHIMA First Department of Anatomy, Kurume University School of Medicine, Kurume 830, Japan Key Words : Comparative anatomy, Formosan monkey, Innervation of the leg. Summary. The mode of nerve supply to the superficial flexor muscles (gastrocnemius, soleus, and plantaris muscles) of the lower leg was studied in a large number of Formosan monkeys (Macaca cyclopis) by gross anatomical inspection. The superficial flexor muscles on the lower leg of primates have generally been reported to be innervated by direct branches from the tibial nerve. However, these muscles in the Formosan monkey were usually found to be supplied by branches from the medial sural cutaneous nerve. The medial sural cutaneous nerve of the Formosan monkey may thus, unlike that in man, be essentially called a musculocutaneous nerve. In addition, the condition of bifurcation of the muscular branches was used to classify the nerve supply of the triceps surae into 8 types, comprising 13 forms. Introduction -Received for Publication, December 4, Determination of the standard type for various traits in animals is a basic prerequisite for comparative anatomical studies. The musculature of the flexor muscles of the leg in primates has been extensively studied. However, most investigations of the nerve supply have been ancillary to examinations of the musculature. With the exception of man, few statistical studies have been made on the nerve supply of primates based on data from a large number of individuals. The nerve supply of the superficial flexor muscles of the lower leg in man was studied statistically by S. Sunderland (1946), M. TOzinbara (1960), etc., and the triceps surae were reported to be normally supplied by direct branches from the tibial nerve. In primates other than man also, the triceps surae are reported to be innervated generally by branches received directly from the tibial nerve (Howell- Straus, 1933; etc.). In contrast, innervation by branches from the medial aural cutaneous nerve is said to represent the normal type of nerve supply in the Formosan monkey (S. Okuda, 1959). Other sporadic reports including those of P. Ssokolow (1933), H. Preuschoft (1962) and Y. El-Assy (1966), although not involving statistical work on large numbers of cases, also mention the nerve supply to the superficial flexor muscles of the lower leg as part of a description of the medial 97

2 98 S. Nagashima sural cutaneous nerve in various animals. In the present study, an attempt was made to overcome the errors which arise from individual differences and variations when studying only a few cases of a single species at an intermediate level among primates. Statistical analyses were made of a large number of individuals to determine the normal type in the Formosan monkey, and the results were compared with previous data for other primates, especially man, obtained by other investigators. The study formed part of a project undertaken by the First Department of Anatomy, Nagasaki University School of Medicine, to determine the standard type of various organs in the Formosan monkey. Materials and Methods The materials used for study comprised both lower limbs of 70 cadavers (38 males, 32 females) selected at random from a collection of adult Formosan monkeys (Macaca cyclopis), the so-called J. Satoh specimens, which are preserved at the Anatomical Laboratory, Nagasaki University School of Medicine. These animals had been fixed by injection of 10% formalin solution into the femoral artery, and were stored in 10% formalin solution. Careful gross anatomical examinations were made in as much detail as possible using a dissecting knife and tweezers. Inspections of minute portions were made using magnifying lenses equipped with an illumination attachment. Findings 1. General Description The sciatic nerve in the Formosan monkey, at about the level of the lower third of the thigh, appeared on the dorsal surface of the adductor magnus in an area lateral to the semimembranosus proprius, and under the cover of the biceps femoris and semitendinosus (figure 1). It then descended along the dorsum of the adductor magnus to the upper part of the popliteal space, where it divided into the common peroneal and tibial nerves, both of which were easily separable as for as the upper thigh. The main trunk of the common peroneal nerve descended obliquely lateralwards across the dorsal surface of the lateral head of the gastrocnemius to the lateral edge of this head, and then sank between the peroneus longus and the flexor digitorum fibularis into the deep portion to supply the anterior and lateral muscle groups of the lower leg. During its downward course, the nerve trunk gave off the lateral sural cutaneous nerve, which pierced the lower part of the biceps femoris to supply the lateral surface of the knee and lower leg as well as the dorsal surface of the lower leg. It was the tibial nerve which supplied all the flexor muscles of the lower leg. After sending off the medial sural cutaneous nerve at the level of the origin of the gastrocnemius, it ran to the lower angle of the popliteal fossa, and sank between the medial head of the gastrocnemius and the plantaris, from behind the popliteal artery and vein. The main trunk of the nerve continued its descent from the lower edge of the popliteus through the lower leg in a shallow groove, which was formed at the boundary between the flexor digitorum tibialis and flexor digitorum fibularis muscles, running side by side with the posterior tibial artery (the nerve being on the Lateral side and the blood vessel on the medial side).. Due to medialward bulging of the muscular belly of the soleus, the nerve passed along the medial edge of the ventral surface of this muscle. During the descent of the nerve trunk through the lower leg, branches were given off to

3 Innervation of the Superficial Flexor Muscles 99 Fig. 1. Condition of bifurcation of the main branches from N. ischiadicus in Macaca cyclopis Abbreviations in figures Am, Adductor magnus ; Bf, Biceps femoris ; Cl, Caput laterale of gastrocnemius ; Cm, Caput mediale of gastrocnemius ; Fdf, Flexor digitorum fibularis ; Fdt, Flexor digitorum tibialis ; Gr, Gracilis ; Ncsl, N. cutaneus surae lateralis ; Ncsm, N. cutaneus surae medialis ; Ni, N. ischiadicus, Npc, N. peroneus communis ; Npl, N. plantaris lateralis ; Npm, N. plantaris medialis ; Npp, N. peroneus profundus ; Nps, N. peroneus superficialis ; Ns, N. Suralis ; Nt, N. tibialis ; P, Plantaris P1, Peroneus longus ; Pc, Popliteus ; Pt, Peroneotibialis ; Ra, Ramus anastomoticus from N. cutaneus surae medialis to N. tibialis ; Rap, Ramus anastomoticus peronaeus ; Sa, Semimembranosus accessorius ; So, Soleus ; Sp, Semimembranosus proprius ; St, Semitendinosus ; Tp, Tibialis posterior ; VI, Vastus lateralis ; Vsp, V. saphena parva ; *, independent cutaneus branch from N. peroneus communis

4 100 S. Nagashima the knee joint capsule and the plantaris in the region of the popliteal fossa, and then, dorsal to the popliteus, muscular branches went to the deep flexor muscles. In the distal portion of the lower leg, a communicating branch from the medial sural cutaneous nerve was received just above the medial malleolus. Then, the main trunk of the tibial nerve divided into the medial and lateral plantar nerves, which arched around the medial malleolus to the sole of the foot from behind the tendon of the flexor digitorum tibialis. The medial sural cutaneous nerve, which was found in all cases examined, was the first branch to separate from the dorsal surface of the main trunk of the tibial nerve within the popliteal fossa, and immediately gave off muscular branches to the triceps surae. It was the largest of the branches originating from the tibial nerve, and very rarely arose independently from the tibial nerve without forming a common trunk with other muscular branches (7/140 cases 5.0 %). The medial sural cutaneous nerve, after sending off muscular branches to the triceps surae, ran from the lower angle of the popliteal fossa to between the two heads of the gastrocnemius, where in most cases it sank into the deep portion of the muscle (deep type ; 131/140, 93.6%). There were, however, rare cases in which it ran along a groove on the surface of the gastrocnemius, beneath the crural fascia (superficial type ; 9/140, 6.4%). In the nerve course of the deep type, the nerve, accompanied by the sural artery, a branch from the popliteal artery, pierced the gastrocnemius at the junction of the two heads (usually at a level slightly below the upper third of the lower leg) to emerge on the dorsal surface of the muscle. The nerve then gently curved lateralwards and downwards to run to about the proximal point of the lower third of the lower leg, where it penetrated the crural fascia and emerged into the subcutaneous region to become the sural nerve. The sural nerve, after giving off the lateral calcaneal branches slightly above the lateral malleolus, arched around the lateral malleolus, and then became the lateral dorsal cutaneous nerve. This supplied the lateral side of the dorsum of the foot and the fifth digit. Just before it pierced the fascia, the medial sural cutaneous nerve gave off a communicating branch to the tibial nerve. This branch, always present in the For mosan monkey, usually arose when the medial sural cutaneous nerve reached the lateral margin of the soleus. The communicating branch turned about 45 and ran medialwards and downwards along the ventral surface of the soleus to immediately above the medial malleolus, where it anastomosed with the distal portion of the main trunk of the tibial nerve. There were sporadic cases in which a communicating branch anastomosed with the lateral plantar nerve (11/140, 7.9%). The nerve branch to the knee joint capsule was usually a very slender branch supplying the medial aspect of the articular capsule in the region of the posterior wall of the articular cavity. It arose most commonly from the tibial nerve just before the point of origin of the muscular branch to the plantaris (102/140, 72.9%). However, it occasionally arose by a common trunk with the muscular branch to the medial head of the gastrocnemius (26/140, 18.6%) or by a common trunk with the muscular branch to the plantaris (12/140, 8.6%). Although not the principal topic of this paper, a description will now be given of a cutaneous nerve which appeared to be characteristic of the Formosan monkey. The medial sural cutaneous nerve, as it descended through the lower leg, did not

5 Innervation of the Superficial Flexor Muscles 101 give off cutaneous branches to the posterior side of the leg except the lateral calcaneal branches. Therefore, the cutaneous nerve supply of the sural region was either by an extension of the branch to the lateral side of the knee from the lateral sural cutaneous nerve or by an extension of the posterior femoral cutaneous branch of the posterior femoral cutaneous nerve. The former condition was more common in the Formosan monkey. The lateral sural cutaneous nerve, after arising from the common peroneal nerve, emerged to the subcutaneous region by piercing the distal portion of the biceps femoris, but an additional independent cutaneous branch to the sural region was frequently seen (figure 1, 32/140, 22.9%). This nerve arose from the common peroneal nerve separately from the lateral sural cutaneous nerve, and more often did not pierce the biceps femoris (26/32, 81.3%), although in rare cases it did penetrate the medial edge of this muscle (6/32, 18.7%). It ran together with the small saphenous vein to terminate at about the middle or at about the level of the lower two thirds of the posterior surface of the lower leg. Such a cutaneous nerve was found in 18.0% of the Formosan monkeys studied by Okuda (1959) who reported it as an independent cutaneous branch. Since it arises separately from the common peroneal nerve and runs to the sural region independently, it seems appropriate to term this nerve the "intermediate sural cutaneous nerve". 2. Innervation of the Gastrocnemius The muscular branches to the gastrocnemius were associated with the branches to the soleus, and generally arose from the medial sural cutaneous nerve, a division of the tibial nerve, although there were a few cases in which the gastrocnemius received a direct branch from the tibial nerve. The details of the nerve supply may be classified into the following 8 types, comprising 13 forms, based on the condition of bifurcation of the muscular branches to the medial and lateral heads of the gastrocnemius and to the soleus. This is illustrated diagrammatically in figure 2. Type 1 : The muscular branches to each head of the gastrocnemius and to the soleus all arise independently from the medial sural cutaneous nerve. Type 2 : The branch to the medial head arises directly from the medial sural cutaneous nerve, and the muscular branches to the lateral head and to the soleus arise by a common trunk from the medial sural cutaneous nerve. 2a The medial head receives a single branch. This 2a type is the most usual form in the Formosan monkey. 21) The medial head receives two slender branches. Type 3 : The muscular branches to the medial head and to the soleus arise by a common trunk, while the branch to the lateral head arises independently from the medial sural cutaneous nerve. Type 4 : The muscular branches to the medial and lateral heads and to the soleus all arise by a common trunk from the medial sural cutaneous nerve. 4a : The muscular branch to the medial head is sent off first, and then the common trunk divides into the muscular branches to the lateral head

6 102 S. Nagashima Fig. 2. Diagrams illustrating the distribution of nerve supply to the triceps surae in Macaca cyclopis,

7 Innervation of the Superficial Flexor Muscles 103 and the soleus. 4b : Division into three muscular branches occurs at about the same location. 4c : The muscular branch to the lateral head is sent off first, and then the common trunk divides into the muscular branches to the medial head and the soleus. Type 5 : The medial head receives an independent branch directly from the tibial nerve, while the muscular branches to the lateral head and the soleus arise by a common trunk from the medial sural cutaneous nerve. Type 6 : The branches to the lateral head and the soleus are given off from the medial sural cutaneous nerve, while the branch to the medial head originates from the tibial nerve, all as independent branches. Type 7 : The muscular branches to the lateral head and the soleus arise by a common trunk from the tibial nerve, while an independent branch to the medial head arises from the medial sural cutaneous nerve. Type 8 : The muscular branches to each head of the gastrocnemius and the soleus are not given off from the medial sural cutaneous nerve but arise from the tibial nerve. 8a : The muscular branches to the lateral head and the Table 1. Frequency by types of nerve supply to the triceps surae

8 104 S. Nagashima soleus arise by a common trunk, while the medial head receives an independent branch. 8b The muscular branch to each head of the gastrocnemius arises by a common trunk, while the soleus receives an independent branch. 8c : Muscular branches to both heads of the gastrocnemius and to the soleus all arise directly as independent branches. The limbs of each case were examined to determine the frequency of these types. The results are summarized in table 1. Fig. 3. Most usual type of nerve supply to the superficial flexor muscles of the leg in Macaca cyclopis. The standard condition in the Formosan monkey was that the muscular branches to the lateral head of the gastrocnemius and to the soleus arose by a common trunk from the medial sural cutaneous nerve, while the medial head of the gastrocnemius was supplied by a branch which arose independently from the medial sural cutaneous nerve (type 2a ; 93/140, 66.4%). This type was followed in frequency by the comparatively many cases in which the muscular branches to these three regions all arose as independent branches from the medial sural cutaneous nerve (type 1; 23/140, 16.4%). A diagram illustrating the normal nerve supply to the superficial flexor muscles of the lower leg in the Formosan monkey is given in figure 3. Clearly, it is very rare in the Formosan monkey for the medial sural cutaneous nerve to separate independently from the tibial nerve without any relation to the muscular branches to the triceps surae, and to reveal characteristics of being a true cutaneous nerve (type 8; 7/140, 5.0%). A muscular branch from the medial sural cutaneous nerve was received by the lateral head of the gastrocnemius in 91.4% of the individual limbs examined (types 1-6 ; 128/140), while a muscular branch was similarly received by the medial head of the gastrocnemius in 92.1% (types 1-4 and 7; 129/140). Muscular branches from the medial sural cutaneous nerve were received simultaneously by both heads of the gastrocnemius in 88.6% of the cases (types 1-4 ; 124/140). The nerve corresponding to the medial sural cutaneous nerve in the Formosan monkey is thus essentially a musculocutaneous nerve. Entry of the muscular branch into the gastrocnemius took place, for each head, immediately below the origin of the muscle (usually at the level of the line of the articular surface) from the medial edge of the ventral surface at a location

9 Innervation of the Superficial Flexor Muscles 105 which was generally symmetrical (figure 3). Furthermore, in cases with the usual type of nerve supply, the muscular branch to the medial head originated from the medial sural cutaneous nerve generally at a point slightly proximal to the separation of the common trunk that supplied the lateral head and the soleus. The muscular branch to the medial head frequently separated into 2 or 3 twigs just before its entry into the muscle, and as mentioned above, there were some cases in which the branch to the articular capsule was given off in association with this branch (26/140). 3. Innervation of the Soleus The muscular branch to the soleus usually arose from the medial sural cutaneous nerve by a common trunk of origin with the muscular branch to the lateral head of the gastrocnemius. However, the detailed conditions of origin may be classified into the following 6 types. Data for each case and limb regarding the frequency of each type are summarized in table 2. Type A : An independent branch is received from the medial sural cutaneous nerve with separation usually occurring at a location slightly distal to the origin of the muscular branch to the lateral head of the gastrocnemius (figure 2, types 1 and 6). Type B : The muscular branches to the lateral head of the gastrocnemius and to this muscle arise by a common trunk from the medial sural cutaneous nerve (figure 2, types 2 and 5). Type C : The muscular branches to the medial head of the gastrocnemius and to this muscle arise by a common trunk from the medial sural cutaneous nerve (figure 2, type 3). Type D: The muscular branches to both heads of, the gastrocnemius and to this muscle all arise by a common trunk from the medial sural cutaneous nerve (figure 2, type 4). Type E : The muscular branches to the lateral head of the gastrocnemius and to this muscle arise by a common trunk from the tibial nerve (figure 2, types 7 and 8a). Type F An independent branch is received directly from the main trunk of the tibial nerve, with separation usually occurring a location slightly distal to the origin of the muscular branch to the gastrocnemius (figure 2, types 8b and 8c). The soleus in the Formosan monkey was supplied by elements from the medial sural cutaneous nerve in the majority of cases (types 1-6 ; 128/140, 91.4%), and it was infrequent for the muscular branch to be received from the tibial nerve (types 7 and 8; 12/140, 8.6%). The muscular branch to this muscle arose Table 2. Frequency by types of nerve supply to the soleus

10 106 S. Nagashima by a common trunk with that to the lateral head of the gastrocnemius in 75.0% of the cases (types 2, 4, 5, 7 and 8a ; 105/140), and with the common trunk being given off from the medial sural cutaneous nerve in 70.7% (types 2, 4 and 5; 99/140). This was followed in frequency by a comparatively large number of cases receiving a branch directly from the medial sural cutaneous nerve (types 1 and 6; 25/140, 17.9%). It was rare for an independent branch to be received directly from the tibial nerve (types 8b and 8c ; 6/140, 4.3%). It can thus be said that in the condition of normal nerve supply, the branch which supplies the soleus in the Formosan monkey arises from the medial sural cutaneous nerve by a common trunk of origin with the muscular branch to the lateral head of the gastrocnemius. The course of the muscular branch to this muscle was stable, and in most cases, after separating from the muscular branch to the lateral head of the gastrocnemius, it descended between the plantaris and the lateral head of the gastrocnemius, in contact with the lateral surface of the plantaris, until it reached this muscle. It then entered from the center of the dorsal surface of the origin of this muscle (figure 3). In most cases, the level of entry of the muscular branch was the level of the upper quarter of the muscle (81.4%). In the remaining cases, entry took place within the upper third of the muscle. There was no double nerve supply to this muscle by the posterior tibial nerve (Hepburn) in the Formosan monkey. 4. Innervation of the Plantaris The plantaris, a muscle always present in the Formosan monkey, was most frequently supplied by an independent muscular branch sent off directly from the tibial nerve (77/140, 55.0%), but there were also many cases in which the nerve supply was associated with the muscular branches that ran to the popliteus, peroneotibialis, and the tibialis posterior muscles of the deep flexor group in the lower leg (figure 4). In the latter cases, the branch to this muscle separated from the tibial nerve at about the same level as the bifurcation of the muscular branch that extended to the deep flexor muscles (43/140, 30.7%) or by a common trunk which during its course sent off the muscular branch to the plantaris (20/140, 14.3%). This muscular branch to the plantaris, after separating from the tibial nerve or 77 cases 43 cases 20 cases (55.0%) (30.7%) (14.3%) Fig. 4. Diagrams of nerve supply to the plantaris.

11 Innervation of the Superficial Flexor Muscles 107 from the muscular branch to certain deep flexor muscles, ran almost vertically in a forward and lateral direction to the origin of this muscle, where it entered into the medial portion or medial border of the ventral surface of the muscle usually at a point less than 2 or 3 cm below the tip of the origin (figure 3). The branch to the articular capsule in the Formosan monkey usually originated directly from the tibial nerve, but there were some cases in which this nerve branch arose by a common trunk with the muscular branch to the plantaris (12/ 140). Comparative Anatomy and General Discussion The tibial nerve in primates is said to separate from the sciatic nerve or arise directly from the lumbosacral plexus. Its composition varies with species. In Macaca, it is reported to contain elements from L5 to S1 (El-Assy) or from L5 to S2 (Howell-Straus). The tibial nerve in the Formosan monkey, similarly to man and many other primates, arises from the sciatic nerve and is easily separable from the common peroneal nerve as far as above the thigh. The report of Kohlbrugge indicates that the tibial nerve in primates is a direct continuation of the sciatic nerve. The first branch to be given off within the popliteal fossa from the tibial nerve in the Formosan monkey is the medial sural cutaneous nerve. This is essentially a musculocutaneous nerve and is larger than any of the muscular branches given off later. Earlier reports generally describe the nerve supply of the triceps surae in primates including man as being by branches directly from the tibial nerve. There are few papers concerning the nerve supply of the triceps surae that can be used for comparison with the present results in which the relationships of the cutaneous nerve corresponding to the medial sural cutaneous nerve in the Formosan monkey were classified into 8 types, comprising 13 forms. A careful review of the literature, however, revealed the statement in the report by Okuda (1959) that the gastrocnemius receives a muscular branch from the madial sural cutaneous nerve : the frequency at which the madial sural cutaneous nerve was found by him to be a purely cutaneous nerve was 9.0% (9/100), which is similar to the value of 5.0% (7/140) in the present study. Even among anthropoid apes, the studies by Ssokolow on the chimpanzee and by Preuschoft on the gorilla have shown that the muscular branches to the triceps surae arise, in common with the medial sural cutaneous nerve, from the tibial nerve in the upper part of the popliteal fossa. Furthermore, the subsequent course of the medial sural cutaneous nerve was found by them to be almost the same as in the Formosan monkey except that this nerve is located superficially to the gastrocnemius. However, other reports on anthropoid apes mention the medial sural cutaneous nerve or sural nerve as being independent in the orang-utan (Ssokolow) and in the gorilla (Raven). El-Assy also indicated on the basis of his examinations of Lemur, Cebus, Ateles, Macaca, Pan, etc. that the gastrocnemius, plantaris, and soleus in these genera receive their nerve supply either from the tibial nerve or from the medial sural cutaneous nerve. There are occasional papers, such as those mentioned above, that include a description of the muscular branches to the superficial flexor muscles of the lower leg which are related to the medial sural cutaneous nerve, but no statistical reports involving large numbers of cases are available for primates other than man. Most reports simply mention the presence of a branch from the tibial nerve.

12 108 S. Nagashima Even when the relationships with the medial sural cutaneous nerve are excluded, the pattern of distribution of muscular branches to the superficial flexor group of the lower leg varies in lower primates. For examble, the tibial nerve in Lemur rufifrons (Glaesmer) sends off a branch which supplies the two heads of the gastrocnemius and the plantaris, and a twig passes between the lateral head of the gastrocnemius and the plantaris to run to the deep portion where it supplies the soleus. In Galago galago (Glaesmer), the tibial nerve sends off two branches just above the knee joint, the medial of which is slender and distributed to the medial head of the gastrocnemius, while the larger lateral branch, which supplies the lateral head and the soleus, and gives rise, within the popliteal fossa, to another branch to the plantaris. In Hapale penicillatus (Glaesmer), the tibial nerve gives rise to a branch which supplies all of the superficial flexor muscles of the lower leg. Furthermore, Okuda (1953) has reported that the tibial nerve of Macaca rhesus gives off three branches all at about the same level, of which the medial branch is distributed to the medial head of the gastrocnemius, and the lateral branch supplies the lateral head of the gastrocnemius and the soleus, while the plantaris usually receives a twig from a branch which arises by a common trunk with the muscular branches to the deep flexor muscles. The normal type of nerve supply in the Formosan monkey is similar to that of the galago and rhesus monkey mentioned above, if the relation to the medial sural cutaneous nerve is not taken into consideration. However, it is suspected that there might also be cases among these lower primates in which the muscular branch separates from the tibial nerve by a common trunk with the medial sural cutaneous nerve. The presumed standard pattern of nerve supply in relation to the course of the muscular branches to the superficial flexor muscles of the lower leg and of the medial sural cutaneous nerve, is compared for man and the Formosan monkey in figure 5. The differences may be summarized as follows. Firstly, there are differences in the pattern of distribution of muscular branches to the superficial flexor muscles as regards the relationship between the muscular branches to the triceps surae and the medial sural cutaneous nerve, whether or not there is a double nerve supply to the soleus, and the state of bifurcation of the muscular branch to the plantaris. Secondly, there are differences in the course of the medial sural cutaneous nerve as regards whether it is superficial or deep in relation to the gastrocnemius, the level at which the deep fascia of the lower leg is penetrated, the mode of composition of the sural nerve, and whether or not there is an anastomosing branch with the tibial nerve. The medial sural cutaneous nerve in both man and the Formosan monkey is the first branch to be given off from the tibial nerve within the popliteal fossa. However, this nerve is a purely cutaneous nerve in man, whereas it is a musculocutaneous nerve in the Formosan monkey. The triceps surae in man receive branches directly from the tibial nerve ; in the Formosan monkey, they receive branches from the medial sural cutaneous nerve. According to the report of Sunderland, the muscular branches to the two heads of the gastrocnemius in man usually arise independently at the same level below the epicondylar line, although there are many other cases in which they arise by a common trunk within the popliteal fossa. In the human fetus, the medial head of the gastrocnemius is frequently found to receive two or more independent branches from the main trunk (TOzinbara),

13 Innervation of the Superficial Flexor Muscles 109 Macaca cyclopis Man Fig. 5. Diagrammatic representation of the standard type for distribution of nerve supply in man and Formosan monkey. but only one such case was encountered in the Formosan monkey. Furthermore, bifurcation of the branch to the articular capsule together with the muscular branch to the medial head is rare in man (TOzinbara, 2/30), but was comparatively frequent in the Formosan monkey. The muscular branch to the soleus in man most commonly has an independent origin from the tibial nerve (Sunderland, 11/20 ; TOzinbara, 19/30), but comparatively many cases are also found to have a common trunk of origin with the muscular branch to the lateral head of the gastrocnemius (Sunderland, 6/20 ; TOzinbara, 8/30). This latter type was noted in the study on the gorilla by Raven. The mode of innervation of the triceps surae described above is the standard type in man and is often also said to be the standard type in anthropoid apes. However, it is found in a small number of cases in the Formosan monkey (figure 2, type 8). Furthermore, it should be noted that the soleus in man, in addition to receiving the branch described above as being given off at a proximal level, usually has a double nerve supply by a second branch that arises either directly from the posterior tibial nerve (Hepburn Sunderland), which is the name given to the tibial nerve after it passes the lower border of the popliteus, or in association with the muscular branch that supplies the deep flexor muscles. This situation as well as the tibial origin of this muscle is a unique feature of man, and is considered to be a secondary change due to the high development of the muscle. No such case was encountered in the

14 110 S. Nagashima Formosan monkey. Usually, only the branch that separates at a proximal level from the medial sural cutaneous nerve was received in the Formosan monkey, and only a proximal division to this muscle is the basic type in many animals. In general, double nerve supply to the soleus does not exist in primates except for man (Glaesmer ; Hepburn ; Kohlbrugge ; Preuschoft ; etc.). However, a double nerve supply may be seen as an exceptional condition in Hylobates leuciscus (Kohlbrugge) and Gorilla gorilla (Raven), although it is not by a branch from the posterior tibial nerve. In the former species, a branch that separates from the upper portion of the tibial nerve (the internal popliteal nerve) enters directly into the soleus. In the latter species, the situation is somewhat unique : the tibial nerve, after giving off two branches to the triceps surae, gives rise to another large branch at a level 3 cm below the knee. This branch sends off muscular branches to the other flexor muscles as it runs downwards parallel with the main trunk of the tibial nerve to the foot. However, during its course a twig is given off that enters the soleus at about its insertion. In man, when there is double nerve supply, the proximal branch enters the dorsal surface of the muscle, while the distal branch enters from the ventral surface (TOzinbara ; Bardeen). It is interesting to note that in many cases of the Formosan monkey, the lateral head of the gastrocnemius and the soleus receive muscular branches which come from the same nerve branch, thus suggesting a close relationship between these two muscles. Supply of the two muscles by nerves which have a common trunk of origin is frequently seen in man and anthropoid apes, as mentioned above. This condition constitutes an absolute majority in the rhesus monkey (Okuda, 1953, 31/34), similarly to the Formosan monkey, and this, at least, appears to be the normal type in Macaca. Muscular differentiation and nerve supply are closely related, so that examinations of the relationships of the nerve supply provide the most important basis for determining the phylogeny of the muscles. According to Bardeen and Uesugi, the skeletal and muscular structures of the limb are differentiated from the mesenchyme of the limb-bud, and the differentiation of the muscles and of the nerves of the limb is generally parallel. However, the muscular anlage is formed somewhat earlier, followed shortly by the passive extension of the nerve to the area of the muscle cell mass which it is to innervate, and then the tissue develops into musculature. Observations on the patterns of nerve supply of local muscles should be made from the foregoing viewpoint, and the findings in the Formosan monkey seem to be indicative of a close relation between the lateral head of the gastrocnemius and the soleus during the developmental stage of these two muscles. In the present study, a unique case was encountered in which the soleus had an excessive origin by a common origin with the lateral head of the gastrocnemius. This strengthened the author's belief that there is an intimate relationship between these two muscles in primates. Furthermore, the muscular branch of the nerve to the soleus in primates has in rare cases been reported to penetrate the muscle belly of the gastrocnemius before entering into this muscle (Hylobates Kohlbrugge ; Macaca inulatta Okuda, 1953), but no such case was noted in the Formosan monkey, with the course of the nerve supply being stable. The muscular branch to the plantaris in both man and the Formosan monkey is generally a direct branch from the main trunk of the tibial nerve. In man, however, it arises from various sites

15 Innervation of the Superficial Flexor Muscles 111 within the popliteal fossa and is usually the first muscular branch to be given off (Sunderland). In contrast, in the Formosan monkey it arises at about the level of the articular line of the knee after the medial sural cutaneous nerve (or rarely a direct branch that goes to the triceps surae) has been sent off. Furthermore, the muscular branch to the plantaris in man is reported to be frequently associated. with the muscular branch to the gastrocnemius (Sunderland). In the Formosan monkey, there was no case with a common origin with other muscular branches to the superficial flexor muscles, and there was rather a tendency for it to be associated with muscular branches to certain deep flexor muscles (the popliteus, peroneotibialis, and tibialis posterior). A review of the state of origin of the muscular branch to the plantaris in lower primates revealed that the condition in the galago (Glaesmer) is the same as the standard type in the Formosan monkey, but in the rhesus monkey it arises from the tibial nerve by a common trunk, with the muscular b ranches to the deep flexor muscles and is the first branch given off from the nerve branch (Okuda, 1953). However, the flexor digitorum tibialis and fibularis usually receive branches directly from the tibial nerve in the Formosan monkey, a finding which is consistent with the observations of Howell-Straus on the rhesus monkey. In man, this muscular branch and the branch to the articular capsule of the knee joint arise in rare cases by a common trunk of origin (TOzinbara, 3/30), and such a condition was likewise seen rarely in the Formosan monkey. The medial sural cutaneous nerve in the Formosan monkey, after giving off muscular branches to the triceps surae, usually runs in the deep portion between both heads of the gastrocnemius to the region where the two heads unite. The nerve pierces this muscle in this area to emerge onto the dorsal surface, and then continues its course lateralwards and downwards to the upper point of the lower third of the leg, where it penetrates the crural fascia to the subcutaneous region and becomes the sural nerve. The medial sural cutaneous nerve in man and anthropoid apes is said to be generally located superficially to the gastrocnemius (Tuda ; Kosinski), but it appears to be the standard condition in other primates for the nerve to run in the deep portion similarly to the Formosan monkey (Ssokolow ; Hill ; El-Assy ; Okuda, 1959 ; etc.). The level at which this nerve penetrates the crural fascia in man is that at which the Achilles tendon begins, i. e. at about the mid-point of the lower leg. This level in anthropoid apes is reported to be lower than in man (Bolk ; Ssokolow ; Kosinski ; etc.), and penetration occurs at an even lower level in the Formosan monkey. The mode of formation and distribution of the sural nerve in man is complicated, and marked differences are said to exist between Oriental races (P'an ; Tuda) and certain European races (Kosinski ; Ssokolow). According to the literature, the structure of the sural nerve can be classified into anastomotic and non-anastomotic types with further subdivisions into 5 subtypes. In the most typical mode in man, it is formed by the union of the medial sural cutaneous nerve with the peroneal anastomotic branch, a branch of the lateral sural cutaneous nerve arising from the common peroneal nerve ; and this union usually occurs in the lower half of the leg. In the Formosan monkey, however, no case was found with an anastomotic branch between elements of the medial sural cutaneous nerve and the lateral sural cutaneous nerve. That is to say, the sural nerve was simply a direct

16 112 S. Nagashima continuation of the medial sural cutaneous nerve, and its peripheral distribution was also simple, becoming the lateral dorsal cutaneous nerve which supplies the lateral margin of the dorsum of the foot and the fifth digit. This is the universal condition in primates except man (Ssokolow ; El- Assy ; Hepburn ; Bolk ; Hill; Preuschoft ; Howell-Straus ; etc.), and it corresponds to the non-anastomotic tibial type of mode of formation of the sural nerve in man. According to Kosinski, formation of the sural nerve by anastomosis of the two above-mentioned cutaneous nerves is not found in animals, even anthropoid apes, and he states that human cases lacking anastomosis should be considered as representing a reversion to the condition in anthropoids. Finally, a communicating branch from the peripheral portion of the medial sural cutaneous nerve to the distal portion of the main trunk of the tibial nerve or to the lateral plantar nerve is said to be present in almost all primates except man and anthropoid apes (Ssokolow ; Hepburn). The Formosan monkey is no exception, and this branch is always present. The communication was with the tibial nerve in the overwhelming number of cases of the Formosan monkey, which was consistent with the findings of Okuda (1959). However, a difference exists among primates in the level of the nerve which receives the communicating branch. There appears to be a difference even within the Cercopithecidae, and the communication is reported to be with the lateral plantar nerve in Macaca mulatta (Howell-Straus ; Ssokolow), Macaca (El- Assy) and Cercopithecus mona (Ssokolow), while it is with the tibial nerve in Cynocephalus hamadryas (Lachmann). Detailed examination of the presence of the independent cutaneous nerve which was frequently found to be distributed to the sural region in the Formosan monkey will be left to future study. Conclusion The superficial flexor muscles of the lower leg were examined in a large number of cases (140 lower limbs) of the Formosan monkey with respect to their nerve supply, in order to determine the normal condition. Interesting findings were obtained, particularly as regards the association with the medial sural cutaneous nerve. A comparison was made with the condition in other primates, principally man, and considerable differences were noted in the pattern of distribution of the muscular branches and in the course of the medial sural cutaneous nerve. The condition in the Formosan monkey may be summarized as follows. 1. The branches given off from the main trunk of the tibial nerve in the leg are usually the medial sural cutaneous nerve, the branch to the knee joint capsule, the muscular branch to the plantaris, and the branches to the deep flexor muscles in that order. 2. The triceps surae usually receive branches from the medial sural cutaneous nerve, and the condition of nerve supply can be classified into 8 types, comprising 13 forms, based on the condition of bifurcation of the muscular branches. a) The muscular branches to the lateral head and to the medial head of the gastrocnemius, respectively, were branches from the medial sural cutaneous nerve in 91.4% and 92.1% of the cases. b) Muscular branches from the medial sural cutaneous nerve were received simultaneously by both heads of the gastrocnemius in individual limbs in 88.6% of the cases. c) The muscular branch received by the soleus originated from elements of the medial sural cutaneous nerve in

17 Innervation of the Superficial Flexor Muscles %, among which it arose from the same trunk of origin with the muscular branch to the lateral head of the gastrocnemius in 70.7%. d) The normal condition of nerve supply of the triceps surae in the Formosan monkey appears to be that in which the medial head of the gastrocnemius is supplied by an independent, direct branch from the medial sural cutaneous nerve, while the lateral head of the gastrocnemius and the soleus receive branches that arise by a common trunk from the medial sural cutaneous nerve. This condition occurred in 66.4% of the cases examined. e) Direct innervation by the tibial nerve, a condition which is considered to be the normal type in man and anthropoid apes, could also be seen in rare cases among the Formosan monkey (5.0%). f) The soleus does not receive a double nerve supply from the distal portion of the tibial nerve in primates other than 'man, and the Formosan monkey was no exception. 3. The plantaris most frequently received an independent, direct branch from the main trunk of the tibial nerve (55.0%), but the branch received in many other cases arose by a common trunk with certain muscular branches to the deep flexor muscles. 4. The medial sural cutaneous nerve is always present in the Formosan monkey. It is the largest branch compared to the other muscular branches that are given off, and is essentially a musculocutaneous nerve. Similarly to many other primates, there was no formation of the true sural nerve by union of this nerve with elements from the lateral sural cutaneous nerve. However, a communicating branch between this nerve and the tibial nerve was always present in the distal portion of the lower leg. 5. An independent cutaneous nerve was frequently found distributed to the sural region in the Formosan monkey (22.9%). This branch is different from the lateral sural cutaneous nerve, and separates from the common peroneal nerve as an independent cutaneous branch which runs together with the small saphenous vein to the middle or lower two-thirds of the lower leg. Ref erences 1) Barden, C. R. & Lewis, W. H. ; Development of the limbs, body-wall and back in man. Am. J. Anat., Vol. 1, p. 1-35, ) Bardeen, C. R. ; Development and variation of the nerves and the musculature of the inferior extremity and of the neighboring regions of the trunk in man. Am. J. Anat., Vol. 6, P , ) Bolk, L. ; Beitrag zur Neurologie der unteren Extremitat der Primaten. Morph. Jb., Bd. 25, S , ) El-Assy, Y. S. ; Beitrage zur Morphologie des peripheren Nervensystems der Primaten. Morph. Jb., Bd. 108, S , ) Glaesmer, E. ; Die Beugemuskeln am Unterschenkel und Fu13 bei den Marsupialia, Insectivora, Edentata, Prosimiae und Simiae. Morph. Jb., Bd. 41, S , ) Hepburn, D. ; The comparative anatomy of the muscles and nerves of the superior and inferior extremities of the anthropoid apes. Part II. J. Anat. Physiol., Vol. 26, P , ) Hill, W. C. 0.; The anatomy of Callimico goeldii (Thomas). Trans. Amer. Philos. Soc., Vol. 49, P , ) Howell, A. B. & Straus, W. L. ; The muscular system. In : The Anatomy of the Rhesus Monkey. edited by Hartman, C. G. and Straus, W. L., Hafner, New York, ) Kohlbrugge, J. H. F. ; Muskeln und periphere Nerven der Primaten, mit besonderer Berucksichtigung ihrer Anomalien. Verh.

18 114 S. Nagashima Akad. Wet. Amsterdam, 2. sect., deel 5, No. 6, 246 pp, ) Kosinski, C. ; The course, mutual relations and distribution of the cutaneous nerves of the metazonal region of leg and foot. J. Anat., Vol. LX, P , ) Lachmann, 0. ; Zur topographischen Anatomie der Hintergliedmae des Hamadryas-Pavians. Z. Morph. Anthrop., Bd. 37, S , ) Okuda Shigeru ; Morphological studies on the muscles of the lower extremities in the Macacus rhesus. Nichidai Igaku Z., Vol. 12, p , (in Japanese) 13) Okuda Syoji ; Cutaneous nerves of the lower extremity of Macacus cyclopsis. Okajimas Fol. Anat. Jap., Bd. 33, S , ) P'an, M. T. ; Formation of sural nerve in the Chinese. Amer. Jour. Physi. Anthrop., Vol. 25, P , ) Preuschoft, H. ; Muskeln und Gelenke der Hinterextremitat des Gorillas. Morph. Jb., Bd. 101, S , ) Preuschoft, H. ; Die Nerven der Hinterextremitat des Gorilla. Anat. Anz., Bd. 110, S , ) Raven, H. C. ; Regional anatomy of the Gorilla. In The anatomy of the Gorilla. Raven memorial volume, Columbia Univ. Press, New York, ) Ssokolow, P. ; Zur Anatomie des N. suralis beim Menschen und Affen. Zeit. Anat. Entw. Ges., Bd. 100, S , ) Sunderland, S. & Hughes, E. S. R. ; Metrical and non-metrical features of the muscular branches of the sciatic nerve and its medial and lateral popliteal divisions. J. Comp. Neur., Vol. 85, P , ) Tazinbara, M. ; Studies on the nerve distribution to the muscles of the lower limb of the Japanese. I: Distribution of the muscular branches to the muscles of the leg. Kadai Igaku Z., Vol. 11, P , (in Japanese) 21) Tuda, M. ; On the N. suralis of the Japanese. Jour. Iwate Med. School, Vol. 3, P , (in Japanese) 22) Uesugi, T. ; Embryological studies on the muscles of the lower extremity in Japanese fetus. Hiroshima Daigaku Kaibogaku Gyosekishu, Vol. 11, P , (in Japanese)