Okajimas Folia Anat. Jpn.. 69(2-3): 77-84, August, 1992

Insertions of the Lumbrical and Interosseous Muscles in the Human

By

Hideki OUKOUCHI, Takuro MURAKAMI and Akio KIKUTA

Section of Human Morphology, Department of Anatomy, Okayama University Medical School, 2-5-1 Shikata-cho. Okayama 700, Japan

-Received for Publications, February 5, 1992-

Key Words: Human foot, Lumbrical muscle, Plantar interosseous muscle, Dorsal interosseous muscle, Dorsal aponeurosis, neurosis, Dorsal digital expansion

Summary: The lumbrical and interosseous muscles in twenty-five feet of Japanese adult cadavers were dissected. The lumbrical muscles mainly continued into the dorsal aponeuroses or the terminal tendons of the extensor digitorum longus muscle, though they occassionally issued some accessory and slender tendons inserting into the bases of the proximal phalanges. Rarely, the lumbrical muscle showed an atavistic anomaly. In this anomaly, the lumbrical muscle was divided into two tails which continued into the bases of the proximal phalanges of the contiguous toes. The plantar and dorsal interosseous muscles were mainly attached to the bases of the proximal phalanges. Frequently, the plantar and dorsal interosseous muscles issued some accessory and small tendons continuing into the dorsal aponeuroses. This fact suggests that the plantar and dorsal interosseous muscles in the foot, like the palmar and dorsal interosseous muscles in the , are composite muscles derived from the flexor brevis, contrahens and other muscles.

The lumbrical muscles of the human foot are human foot (Fig. 1, 2, 3). These muscles were num- generally regarded as being inserted into the pro- bered from the medial side of the foot (Figs. 1, 2, 3). ximal phalanges (Henle, 1871; Frohse and Frãnkel, No morphological difference of the lumbrical, dorsal 1913; Paturet, 1951; Mortenson and Pettersen, 1966; interosseous and plantar interosseous muscles was Gardner, Gray and O'Rahilly, 1971; Tillman and observed between the male and female cadavers and TOndury, 1987). However, our recent dissection also between the right and left feet. of Japanese feet has revealed that the lumbrical The dorsal aponeurosis of the toe consisted of the muscles mainly end in the dorsal aponeuroses. These tendons of the extensor digitorum longus and brevis are reported in the present paper. The insertions of muscles and the outer and inner tendinous mem- the interosseous muscles are also described and dis- branes arising, together with the deep plantar meta- cussed in relation to their phylogenetic compositions. tarsal ligaments, from the plantar aspect of the neck of the metatarsal bone (Figs. 4, 5, 6). The inner tendinous membranes ran around the neck of the Materials and Methods metatarsal bone, and enclosed the tendons of the extensor digitorum longus and brevis muscles at a Twenty-five feet of Japanese adult cadavers of level between the neck of the metatarsal bone and both sexes, which had been fixed with 10% formalin the head of the proximal phalanx (Fig. 5). Thus, the by vascular perfusion and dehydrated with 60-70% inner tendons extended bilaterally along the proxi- ethanol, were dissected with sharpened forceps under mal phalanx (wing tendons) (Figs. 4, 6). The outer a dissection light microscope. tendinous membrane was thick and band-like, and firmly surrounded the plantar and dorsal interosseous muscles and the enclosed tendons of the extensor Results muscles (see above) (Figs. 5, 6). This band-like outer membrane (annular ligament) only extended at a There were four lumbrical, four dorsal interos- level of the neck of the metatarsal bone (Figs. 4. 6). seous and three plantar interosseous muscles in the The lumbrical muscles arose from the tendons of

Address for correspondence: Takuro Murakami, Human Morphology Section, Department of Anatomy, Okayama University Medical School, 2-5-1 Shikata-cho, Okayama 700, Japan.

77 78 H. Oukouchi et al .

Fig. 2. Arrangements, origins and insertions of the dorsal inter- osseous muscles in the human foot (right foot Fig. 1. Schematicdiagram showing the arrangements , plantar , origins aspect). D1—D4 first to fourth dorsal interosseous muscles and insertionsof the lumbricalmuscles in the human foot . MB metatarsal bones, PP proximal phalanges. (rightfoot, plantar aspect). L1—L4 first to fourthlumbrical muscles.DP distal phalanges,FH tendonof the flexor at a level of the metatarso-phalangeal joints, some hallucislongus muscle, FL tendons of the flexordigitorum accessory and slender tendons which were inserted longusmuscle, MB metatarsalbones, MP middle phal- into the bases or basal portions of the proximal anges,PP proximalphalanges, WT wingtendons of the phanges (Fig. 4) (Table 1). dorsalaponeuroses. In one of the twenty-five feet, the third and fourth lumbrical muscles were divided into two (medial the flexor digitorum longus muscle, as far back as and lateral) tails, which reached the contiguous their angles of separation, and, with the exception sides of the adjacent fingers (Fig. 7). More strictly, of the first one which arose only from the medial the medial and lateral tails of the fourth lumbrical border of the first tendon of the flexor digitorum muscle and the lateral tail of the third lumbrical longus muscle, each sprang from two adjacent ten- muscle were further divided into the two tendons dons (Fig. 1). which were inserted into the wing tendons of the The lumbrical muscles ran plantar to the deep dorsal aponeuroses and the bases of the proximal plantar metatarsal ligaments, and ended, at a level phalanges; the medial tail of the third lumbrical of metatarsophalangeal joints, in tendons which, muscle was solely inserted into the base of the pro- passed distally on the medial sides of the four lesser ximal phalanx (Fig. 7). toes and formed the distal ridges of the medial wing The dorsal interosseous muscles were bipennate tendons (see above) of these toes (Figs. 1, 4, 6). muscles, each arising by two heads from the adjacent Occasionally, the tendons of the lumbrical muscles sides of two metatarsal bones; the first one reached were attached to or mixed with the medial terminal the medial side of the second toe, the other three tendons of the extensor digitorum longus muscle, ones passing to the lateral sides of the second, third and inserted into the dorso-proximal parts of middle and fourth toes (Fig. 2). The plantar interosseous and distal phalanges (Fig. 4). In addition to these muscles arose from the bases and medial sides of the insertions, the lumbrical muscles occasionally issued, third, fourth and fifth metatarsal bones, and reached Lumbrical and Interosseous Muscles in the Human Foot 79

Fig. 3. Arrangements, origins and insertions of the plantar interosseous muscles in the human foot (right foot, plantar aspect). P1—P3 plantar interosseous muscles. MB Meta- tarsal bones, PP proximal phalanges.

Fig. 4. Dorsal aponeurosis of the third toe (right foot, dorsal aspect). Note that the dorsal aponeurosis (DA) was formed by the tendons of the extensor digitorum longus (EL) and brevis (EB) muscles and the outer (OL) and inner (IL) membranous ligaments arising from the plantar aspect of the metatarsal bone (MB). The distal and bilateral segments of the inner ligment are referred to as the wing tendons (WT). Also note that the second lumbrical muscle (L2) ends in the tendon (thick arrowhead), which forms the distal ridge of the medial wing tendon and continues into the medial terminal tendon of the extensor digitorum longus muscle, and that this lumbrical muscle issues an accessory and slender tendon (thin arrowhead) which is inserted into the base of the proximal phalanx. Further- more, it should be noted that the third dorsal (D3) and first plantar (P1) interosseous muscles are attached to the bases of the proximal phalanx (thick arrow), and that the first plantar interosseous muscle issues a small slip (thin arrow) continuous with the wing tendon. DP distal phalanx, LT lateral terminal tendon of the flextor digitorum longus muscle, MT medial teminal tendon of the flexor digitorum longus muscle, MP middle phalanx, PP proximal phalanx, TL deep transverse metatarsal ligament. 80 H. Oukouchi et al.

Table 1. Combinations and occurrence of main and accessory tendons of the first to forth lumbrical muscles (L1—L4) in 25 human feet. The main tendon (M) is inserted into the wing tendon of the dorsal aponeurosis or mixed into the medial terminal tendon of the extensor digitorum longus muscle, while the accessory one (A) is attached to the base of the proximal phalanx (see text). Aberrant cases are shown in Figure 7 (see text)

Lumbrical Muscles

the medial sides of the same toes (Fig. 3). The dorsal and plantar interosseous muscles ended, just proximal to the metatarsophalangeal Fig. 5. Dorsal aponeurosis (transeversely cut form, at a level of joints, in their terminal tendons which were attached the neck of the third metatarsal bone, right foot, proximal to the bases of the proximal phalanges (Figs. 2, 3, 4) aspect). Note that the dorsal aponeurosis (DA) is formed (Table 2). In addition to these main insertions, the by the outer (OL) and inner (IL) membranous ligaments dorsal and planter interosseous muscles frequently continuous with the deep plantar metatarsal ligament (TL). gave off, near the metatarsophalangeal joints, some EL and EB tendons of the extensor digitorum longus and accessory and small tendons or slips which were brevis muscles, D3 and P1 third dorsal and first plantar inserted into the wing tendons of the dorsal apo- interosseous muscles, L2 second lumbrical muscle, MB neuroses (Fig. 4) (Table 2). third metatarsal bone.

sules of the metatarsophalangeal joints. These find- Discussion ings are consistent with the descriptions of the pre- vious authors, including Henle (1871). However, few The present study reveals that the lumbrical authors have described the additional insertions of muscles of the human foot have constant and thick the interosseous muscles into the dorsal aponeuroses insertions into the dorsal aponeuroses of the toes, of the toes or into the capsules of the metatarso- though they occasionally have some accessory and phalangeal joints. slender insertions into the bases of the proximal The dorsal aponeurosis of the toe is sometimes phalanges. These findings are consistent with the referred to as the dorsal digital expansion (Warwick descriptions of Hollinshead (1958), Romanes (1964), and Williams, 1973). However, its details are not Warwick and Williams (1973) and some other authors, clear (or were neither described nor illustrated by and disagree with the usual or traditional textbook the previous authors). We regarded the dorsal apo- descriptions since Henle (1871) that in the human neurosis of the third toe as the representative, and foot, the lumbrical muscles are mainly inserted showed its schematic diagrams in Figures 4 and 5. into the bases of the proximal phalanges or into These diagrams indicate that dorsal aponeurosis in the capsules of the metatarsophalangeal joints the foot is similar to that in the hand (Landsmeer, (Gegenbaur, 1899; Frohse and Frankel, 1913; 1955), and confirm that the terminal tendons of the Paturet, 1951; Mortenson and Pettersen, 1966; extensor brevis muscle join the dorsal aponeurosis Gardner, Gray and O'Rahilly, 1971; Outi, 1982; and finally continue, together with the lateral ter- Tillmann and TOndury, 1987). minal tendons of the extensor digitorum longus The present study also confirms that the plantar muscle, into the bases of the middle and distal and dorsal interosseous muscles in the human foot phalanges from the dorsal aspects (Fig. 4). are constantly and mainly inserted into the bases of We have recently studied the human , and the proximal phalanges, though they occasionally confirmed that the lumbrical muscles in the human issue some accessory or small slips which are inserted hands are constantly inserted into the wing tendons into the dorsal aponeuroses of the toes or the cap- of the dorsal aponeusoses, though they occasionally Lumbrical and interosseous Muscles in the Human Foot 81

have some accessory insertions into the bases of the proximal phalanges (Ikebuchi, Murakami and Ohtsuka, 1988). Thus, our studies show that the insertion-patterns of the lumbrical muscles are quite similar in the human hand and foot. We have also studied the hands or forepaws of the kangaroo, dog, cat and monkey, and suggested that the lumbrical muscles in the hands are originally bipennate muscles, which are inserted by two (medial and lateral) tails into the bases of the proximal phalanges of the contiguous fingers (Ikebuchi, 1992). Namely, we have indicated that in the phylogenetic development, the lumbrical muscles lose their lateral tails (or solely remain their medial tails) and also move (or transfer) their insertions from the proximal phalanges to the dorsal aponeuroses. These may suggest that such lumbrical muscles with two tails and insersions into the bases of the proximal phal- anges as shown in Figure 7 are the atavistic anomalies. Lewis (1965) reviewed the phylogenetic history of the interosseous muscles in the hand, and described the primitive mammalian (marsupial) precursors of these muscles as having a bilamilar arrangement: a dorsal layer of bipennate dorsal abductor muscles with the insertions into the bases of the proximal phalanges is overlaid ventrally by a sheet of the flexor brevis muscles with the insertions into the wing tendons of the dorsal digital expansions. He

Fig. 6. Photographof a dissectedform of the third toe (right foot, medialaspect). Note that the secondlumbrical muscle (L2) ends in the tendious membrane (arrowhead) which is continuouswith the wing tendon (WT) of the dorsal aponeurosis(DA). DP distal phalanx, EL tendon of the extersordigitorum longus muscle, FB tendon of the flexor digitorumbrevis muscle, FL tendon of the flexordigitorum longusmuscle, IL inncr ligamentof the dorsalaponeurosis. MB third metatarsalbone, MP middle phalanx. OL outer ligamentof the dorsal aponeurosis, P1 first plantar inter- osseousmuscle, PP proximalphalanx. TL deep transverse metatarsalligament.

Table 2. Combinations and occurrence of the main and accessory tendons of the first to third plantar interosseous muscles (PI —P3) and the first to fourth dorsal interosseous muscles (D1—D4) in 25 human feet. The main tendon (M) is attached to the base of the proximal phalanx, while the accessory one (A) is inserted into the wing tendon of the dorsal aponeurosis (see text).

Intcrosseous Muscles 82 H. Oukouchi et al.

also stated that in the phylogenetic development, the dorsal abductor muscles show a tendency to merge with the subjacent flexor brevis muscles, and that the human dorsal interosseous muscles resulting from the amalgamation of the flexor brevis muscles with the dorsal abductor muscles (Lewis, 1965). We have recently extended or modified the con- cept of Lewis (1965), by taking the contrahens muscles into consideration, and contented that the human palmar interosseous muscles are com- posite muscles derived from the flexor brevis and contrahens muscles, and that the human dorsal interosseous muscles are composite muscles derived from the flexor brevis, dorsal abductor and con- trahens muscles (Ikebuchi, Murakami and Ohtsuka, 1988; Yamamoto; Murakami and Ohtsuka, 1988). Few phylogenetic informations on the interos- seous muscles in the foot have been available. However, the present study shows a fact that the plantar and dorsal interosseous muscles in the foot, like the palmar and dorsal interosseous muscles in the hand (Ikebuchi, Murakami and Ohtsuka, 1988), have additional or accessory insertions into the wing tendons or capsules of the metatarsophalangeal joints. This fact may suggest that the plantar and dorsal interosseous muscles in the human foot are also the composite muscles derived from the dorsal abductor, flexor brevis or contrahens muscles. The dorsal abductor and flexor brevis muscles in the foot may be commonly referred to as the deep flexor brevis muscles (Mm. flexores brevis profundi) (Ribbing, 1938).

References 1) Frohse, F. & Frankel, M.: BardelebenHandbuch der Anatomicdes Menschen.Die Muskeln des Menschlichen Beines.579-613. Gustav Fischer, Jena, 1913. 2) Gardner, E., Gray, D. J. & O'Rahilly, R.: Anatomy. A RegionalStudy of HumanStructure. 252-254. W. B. Saunders,Philadelphia/Toronto/London. 1971. 3) Gegenbaur,C.: Lehrbuchder Anatomic des Menschen. SiebenteVerbesserte Auflage. Erster Band. 475-478. WilhelmEngelmann, Leipzig, 1899. 4) Henle,J.: Handbuchder systematischen Anatomic des men- schen. Muskellehre. Zweite Auflagc. 314-326, Friedrich Viewegand Sohn,Braunschweig, 1871.

Fig.7. Lumbricalmuscles showing atavistic anomalies (female, rightfoot, plantar aspect). Note that eachof the third and forthlumbrical muscles (L3 and L4) givesoff the medial (m) and lateral (1) tails, and that a part of these tails is insertedinto the base of the proximalphalanx (PP) (arrowhead).FL Tendonsof the flexordigitoruin longus muscle,L2 second lumbrical muwle, MB metittarill bones, WTwing tendon. Lumbrical and Interosseous Muscles in the Human Foot 83

5) Hollinshead, W. H.: Anatomy for Surgeons. Vol . 3. The Vol. I. (ed. by T. Ogawa, 0. Mori, T. Mori & H. Outi). Back and Limbs. 870-875. Happer & Row, New York/ 417-427. Kanehara Publishing, Tokyo, 1982. Evanston/London, 1958. 12) Paturet, 6.: Traite d'Anatomie Humaine. Tome II. 6) Ikebuchi, Y.: A comparative study of the lumbrical muscles Membres Superieur et Inferieur. 874-806. Masson & Cie. in the hand (Japanese text). Okayama-Igakkai-Zasshi 104: Paris, 1951. (in press), 1992. 13) Ribbing, L.: Unterschenkel- und Fussmuskulatur. In: 7) Ikebuchi, Y., Murakami, T. & Ohtsuka, A.: The interns- Handbuch der vergleichenden Anatomic der Wirbeltiere. seous and lumbrical muscles in the human hand, with special (ed. by L. Bolk, E. Goppert, E. Kallius & W. Lubosch). reference to the insertions of the interosseous muscles . Acta 624-652. Urban & Schwarzenberg, Berlin/Wien, 1938. Med. Okayama 42: 327-334, 1988. 14) Romanes, G. J.: Cunningham's Textbook of Anatomy. 8) Landsmeer, J. M. F.: The anatomy of the dorsal aponeurosis Tenth ed. 367-369. Oxford University Press, London, 1964. of the human finger and its functional significance . Acta 15) Tillmann, B. & TOndury, G.: Rauber/Kopsch Anatomie Anat. Suppl. 24: 31-44, 1955. des Menschen. Lehrbuch und Atlas. Band I. Bewegungsap- 9) Lewis, O. J.: The evolution of mm. interossei in the primate parat. 626-638. Georg Thieme, Stuttgart/New York, 1987. hand. Anat. Rec. 153: 275-288, 1965. 16) Warwick, R. & Williams, P. L.: Gray's Anatomy. 35th 10) Mortenson, 0. & Pettersen, J. C.: Musculature of the foot. ed. 581-583. Longman, Edinburgh, 1973. In: Morris's Human Anatomy. Twelfth ed. (ed. by B. J. 17) Yamamoto, C., Murakami, T. & Ohtsuka, A.: Homology Anson), 599-609. McGraw-Hill Book, New York/Toronto/ of the adductor pollicis and contrahentes muscles: a study of Sydney/London, 1966. monkey hands. Acta Med. Okayama 42: 215-226, 1988. 11) Outi, H.: Musculi pedis (Japanese text). In: Anatomy.