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Keywords:

  • obturator internus;
  • quadratus femoris;
  • gemelli muscles;
  • innervation;
  • sacral plexus;
  • human gross anatomy;
  • comparative morphology

Abstract

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

The manner of innervation of the obturator internus, superior and inferior gemelli, and the quadratus femoris in humans (101 pelvic halves) and in rhesus monkeys (Macaca mulatta: 8 pelvic halves) were investigated. In most specimens, the inferior gemellus originated from the lateral surface of the ischial tuberosity and also from the medial surface (intrapelvic origin) just beneath the obturator internus and was covered by the falciform process of the sacrotuberous ligament. The superior gemellus was frequently innervated by the nerve to the obturator internus and the nerve to the quadratus femoris (60.4%), and the inferior gemellus was innervated by the obturator internus nerve in two specimens. The quadratus femoris nerve originated from more cranial segments than the obturator internus nerve, however these nerves had various communication patterns inside and outside the muscles. According to the intramuscular nerve distribution, in some specimens the branches to the superior gemellus from the quadratus femoris nerve extended to the inferior gemellus, and the branches to the inferior gemellus were distributed to the obturator internus. The present findings revealed that the positional relationships among the branches to the obturator internus and gemelli muscles are relatively constant, although the branching patterns and innervation patterns were varied. The various patterns and routes are considered to reflect the variability of the differentiation patterns of the anlage of the muscles. A possible schematic model of the positional relationships between the muscles and the nerves is proposed. Anat Rec 263:41–52, 2001. © 2001 Wiley-Liss, Inc.

The obturator internus, quadratus femoris and gemelli are deep muscles of the hip joint. Several comparative anatomical studies have described the quadratus femoris (Cunningham, 1881; Wilson, 1888; Bardeen, 1907), however, few reports introduce the details of the obturator internus and gemelli muscles. Gräfenberg (1904) and Bardeen (1907) proposed that these muscles are derived from a common muscle anlage, and the obturator internus shifts to the intrapelvic space to cover the obturator foramen. Kikuchi (1987b) described that the superior gemellus is supplied not only by the nerve to the obturator internus (obturator internus nerve) but also by the nerve to the quadratus femoris (quadratus femoris nerve), and thus he proposed that the superior gemellus has two different origins. Recently, however, Shinohara (1995) proposed that the obturator internus and the two gemelli represent three heads of one muscle according to the muscle formation and innervation findings. In addition, Honma et al. (1998) reported a communication between a branch to the inferior gemellus from the quadratus femoris nerve and a branch of the obturator internus nerve within the obturator internus muscle, and recognized these muscles to be part of the same muscle mass. Further, embryological studies (e.g., Bardeen, 1907) support these findings and suggest the possibility of numerous communicating branches in accordance with their close positional relationship. In the present study, we found such communicating branches among these muscles. We propose a possible scheme to explain the positional relationships between the muscles and the branches of the innervating nerves based on our findings.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

To investigate the innervation patterns of the obturator internus, superior and inferior gemelli and quadratus femoris muscles, 101 pelvic halves of 60 human cadavers were dissected. After removing the glutei maximus and medius, the origins, courses and branching patterns of the nerve to the quadratus femoris (quadratus femoris nerve) and the nerve to the obturator internus (obturator internus nerve) were examined. In 39 pelvic halves of 20 cadavers, the obturator internus, gemelli and quadratus femoris muscles were removed from bones with their innervating nerves, and the lumbar and sacral plexuses were minutely analyzed to reveal the segmental composition of the nerves. Furthermore, to investigate the nerve communication within the muscles, the intramuscular nerve distribution to these muscles in eight pelvic halves was examined in detail under a binocular microscope and then recorded. During investigation of two specimens, it was observed that a branch from the quadratus femoris nerve innervated the adductor magnus muscle. In these specimens, the intramuscular nerve distribution to the adductor magnus muscle was investigated.

The innervating nerves of the obturator internus, gemelli and the quadratus femoris were dissected in eight pelvic halves of four rhesus monkeys (Macaca mulatta) to compare with those in humans. After complete removal of the bony elements, the branching patterns and segmental composition of the nerves and the intramuscular nerve distribution to the muscles were carefully examined under a binocular microscope.

RESULTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

Humans

Form, origin, and insertion of the obturator internus and the gemelli.

The form, origin and insertion were as typically described (Fig. 1), however, here we describe specific details of the characteristics of the obturator internus and the gemelli. The muscular fibers of the obturator internus converged to form tendinous bands (Fig. 2). These were evident when viewed from the lateral (parietal) surface of the pelvic portion of the muscle (Fig. 2B). In our findings, the formation of these bands was most interesting. The tendinous bands emerged from within the muscle and remained surrounded by muscular fibers for a short distance. This fiber coverage extended more distally at the lower margin. In two specimens, this extension of the obturator internus muscle fibers continued to join the inferior gemellus (Fig. 2B).

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Figure 1. Medial view of the obturator internus muscle in man. Right side. The obturator internus muscle is attached to the inferior gemellus muscle, and the lower margins of these muscles are covered by the falciform process of the sacrotuberous ligament (indicated by an asterisk). CO, coccygeus muscle; IG, inferior gemellus muscle; IT, ischial tuberosity; OI, obturator internus muscle; SS, sacrospinous ligament; ST, sacrotuberous ligament.

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Figure 2. An example of the obturator internus and gemelli muscles in man. Right side. A: Posterior surfaces of the gemelli muscles and the medial surface of the obturator internus muscle. B: Anterior surfaces of the gemelli muscles and the lateral surface of the obturator internus muscle. IG, inferior gemellus muscle; OI, obturator internus muscle; SG, superior gemellus muscle.

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The superior gemellus, before insertion into the greater trochanter, actually first inserted into the anterosuperior surface of the obturator internus tendon. At its origin, however, the superior gemellus was clearly separate from the obturator internus (Fig. 2B).

In most specimens, the inferior gemellus originated from the lateral surface of the ischial tuberosity and also from the medial surface (intrapelvic origin) just beneath the lower margin of the obturator internus and was covered by the falciform process of the sacrotuberous ligament (Fig. 1). The two gemelli were clearly divided on the anterior surface of the obturator internus tendon, and were frequently adjoined on the posterior surface (Fig. 2).

Nerves to the obturator internus and to the quadratus femoris.

The nerve to the quadratus femoris (quadratus femoris nerve) ran on the anterior surface of the gemelli muscles, and innervated the quadratus femoris from the anterior surface. The nerve to the obturator internus (obturator internus nerve) ran on the posterior surface of the sacrospinous ligament, turned to enter the lesser sciatic foramen, and was distributed to the obturator internus from the pelvic surface. During the courses of these two nerves, various branching patterns to the gemelli were observed.

Some roots of the quadratus femoris nerve and the obturator internus nerve frequently formed a common root (84.6% in 33 of 39 sides). In detailed fiber analyses of these common roots from the sacral plexus the components could not be distinguished. Also communication between the obturator internus nerve and the quadratus femoris nerve was frequently observed. Taken together, at least one type of communication between these two nerves was found in all specimens.

The segmental composition of the nerves to the quadratus femoris and to the obturator internus was analyzed (Fig. 3). The quadratus femoris nerve arose from the ventral surface of (L4), L5 and S1 in 79.4%, and the obturator internus nerve arose from the ventral surface of (L5), S1, S2 and (S3) in 84.6% (Table 1). As a root of the quadratus femoris nerve originated from the 4th lumbar nerve, the quadratus femoris nerve was formed by the cranial-most root of the sacral plexus. Therefore, from the viewpoint of segmental composition, the quadratus femoris nerve arose more cranially than the obturator internus nerve.

Table 1. Segmental composition of the nerves to the quadratus femoris and the obturator internus in man
 Quadratus femoris nerveObturator internus nerve
LeftRightSumLeftRightSum
L4 L52 (10.0%)3 (15.8%)5 (12.8%)
L4 L5 S13 (15.0%)4 (21.0%)7 (17.9%)
 L51 (5.3%)1 (2.6%)
 L5 S114 (70.0%)10 (52.6%)24 (61.5%)2 (10.0%)3 (15.8%)5 (12.8%)
 L5 S1 S21 (5.0%)1 (5.3%)2 (5.1%)4 (20.0%)6 (31.6%)10 (25.6%)
 L5 S1 S2 S38 (40.0%)3 (15.8%)11 (28.2%)
  S1 S22 (10.0%)2 (10.5%)4 (10.3%)
  S1 S2 S34 (20.0%)4 (21.0%)8 (20.5%)
  S1 S2 S3 S41 (5.3%)1 (2.6%)
20 (100.0%)19 (100.0%)39 (100.0%)20 (100.0%)19 (100.0%)39 (100.0%)
Innervation patterns of the superior and inferior gemelli.

The inferior gemellus was innervated by branches of the quadratus femoris nerve from the anterior (or deep) surface in all specimens. In two specimens, the muscle was additionally innervated by branches of the obturator internus nerve (Fig. 4B). In one specimen, a branch of the obturator internus nerve first pierced the posteriormost muscle bundle of the obturator internus, and entered the upper surface of the inferior gemellus (Fig. 4A). In another specimen, a branch ran between the obturator internus and the inferior gemellus, and entered the upper surface of the latter muscle (Fig. 4B).

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Figure 3. Composition and ramification of the sacral and pudendal plexuses in man (ventral aspect). Specimen 5 (left, male). Ig, inferior gluteal nerve; L, lumbar nerve; Oi, obturator internus nerve; Pd, pudendal nerve; Per, common peroneal nerve; Pfc, posterior femoral cutaneous nerve; Qf, quadratus femoris nerve; S, sacral nerve; Sg, superior gluteal nerve; Tib, tibial nerve.

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Figure 4. Posterior view of the gemelli muscles in man. The inferior gemellus is innervated by branches from the nerve to the obturator internus (indicated by an arrowhead) as well as by branches of the quadratus femoris nerve. The branch entered the inferior gemellus muscle from the superior surface. A: Specimen 4 (right). B: Specimen 6 (left). IG, inferior gemellus muscle; IT, ischial tuberosity; OI, obturator internus muscle; Oi, obturator internus nerve; Pd, pudendal nerve; QF, quadratus femoris muscle; Qf, quadratus femoris nerve; SG, superior gemellus muscle; Tib, tibial nerve.

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The superior gemellus was innervated by branches of the obturator internus nerve, branches of the quadratus femoris nerve and twigs from the communication of these two nerves. The branches from the obturator internus nerve arose near the ischial spine, ran latero-inferiorly, and entered the posterior (or superficial) surface of the superior gemellus, whereas those from the quadratus femoris nerve entered the anterior surface. The twigs of the communicating branch ran on the upper surface of the muscle, and entered the anterior, superior and posterior surfaces. The innervation patterns of the gemelli muscles are compiled in Table 2; in many specimens the superior gemellus was innervated by both the obturator internus nerve and the quadratus femoris nerve (60.4%). According to the detailed analyses of the sacral plexus, the branches to the superior gemellus, that entered the anterior surface, arose from more cranial segments than those entering the posterior surface (Table 3).

Table 2. Origins of the branches to the superior gemellus and the inferior gemellus in man*
 Branches to the superior gemellusBranches to the inferior gemellus
LeftRightSumLeftRightSum
  • *

    Qf, the branches originated only from the nerve to the quadratus femoris; Qf + Oi, the branches originated from both the nerve to the quadratus femoris and the nerve to the obturator internus; Oi, the branches originated only from the nerve to the obturator internus.

Qf4 (7.7%)4 (8.2%)8 (7.9%)51 (98.1%)48 (98.0%)99 (98.0%)
Qf + Oi34 (65.4%)27 (55.1%)61 (60.4%)1 (1.9%)1 (2.0%)2 (2.0%)
Oi14 (26.9%)18 (36.7%)32 (31.7%)
52 (100.0%)49 (100.0%)101 (100.0%)52 (100.0%)49 (100.0%)101 (100.0%)
Table 3. Segmental composition of the branches to the quadratus femoris, superior and inferior gemelli and obturator internus muscles in man*
SpecimenQfIgSgaOiSgp
  • *

    Qf, branches to the quadratus femoris; Ig, branches to the inferior gemellus; Sga, branches to the superior gemellus which enter from the anterior surface; Oi, branches to the obturator internus; Sgp, branches to the superior gemellus which enter from the posterior surface.

1L4 L5 L5 L5L5 S1L5 S1
2L4 L5L4 L5L4 L5 S1L5 S1 S2 S1 S2
3L4 L5L4 L5L4 L5 S1L5 S1 S2 S3 S1 S2 S3
4L4 L5 S1L4 L5 S1L4 L5 S1 S1 S2 S1 S2
5L4 L5 S1L4 L5 S1L5 S1 S2 S1 S2
6L4 L5 S1 L5 S1 L5 S1 S1 S2 S3  S2 S3
7L4 L5 S1 L5 S1 L5 S1 S1 S2 S3  S2 S3
8L4 L5 S1 L5 S1 S1 S2 S3  S2 S3
9 L5 L5 S1 L5 S1 S1 S2  S2
10 L5 L5 S1L5 S1 S2 S3 S1 S2 S3
11 L5 S1 L5 S1 L5 S1L5 S1 S2 S1 S2
12 L5 S1 L5 S1 L5 S1 S1 S2 S3  S2 S3

The quadratus femoris nerve entered the muscle from the anterior surface in all specimens. In two specimens, a branch of the quadratus femoris nerve extended to the adductor magnus; this branch arose near the upper margin of the quadratus femoris and entered the posterior surface of the adductor magnus. Interestingly, this branch arose from the cranial most segment of the quadratus femoris nerve. In general, the adductor magnus was innervated by branches of the obturator nerve that entered the anterior surface. In these specimens, detailed investigation of the nerve distribution revealed that a twig of the branch from the quadratus femoris nerve communicated with a twig of the obturator nerve within the adductor magnus (Fig. 5A). In addition, according to the detailed fiber analyses of the origin of the obturator nerve, the root of the branches to the adductor magnus occupied the caudal most region of the obturator nerve, and frequently formed a common trunk with the root of the quadratus femoris nerve (Fig. 5B).

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Figure 5. A case where a branch from the quadratus femoris nerve innervates the adductor magnus (left, ventral aspect). A: Intramuscular nerve distribution of the adductor magnus viewed from the anterior surface in man. Ventral aspect. In this specimen, the adductor magnus is innervated by the quadratus femoris nerve as well as by the obturator nerve. In addition, both nerves communicate within the muscle. B: Composition and ramification of the lumbosacral plexus according to fiber analyses. The root of the branches to the adductor magnus is in close proximity to the root of the quadratus femoris nerve. Ab, branch to adductor brevis; Al, branch to adductor longus; AM, adductor magnus; Am, branch to adductor magnus; Fe, femoral nerve; Gf, genitofemoral nerve; Ig, branch to inferior gemellus; L, lumbar nerve; Lfc, lateral femoral cutaneous nerve; Ob, obturator nerve; Oi, branch to obturator internus; Pd, pudendal nerve; Per, common peroneal nerve; Qf, quadratus femoris nerve; S, sacral nerve; Sga, branch to superior gemellus from anterior surface; Sgp, branch to superior gemellus from posterior surface; Tib, tibial nerve.

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Intramuscular nerve distribution of the obturator internus and the gemelli muscles.

Various patterns of intramuscular nerve distribution of the obturator internus and gemelli muscles were observed. In all specimens, the branches of the obturator internus nerve entered the medial surface of the muscle, and spread out anteriorly within the muscle, however some twigs turned to run lateroposteriorly. Various patterns of communication were observed between branches of the obturator internus nerve and those of the quadratus femoris nerve within the superior and inferior gemelli. In addition, branches to the superior gemellus from the quadratus femoris nerve also innervated the inferior gemellus in some specimens.

Typical examples of nerve communications are described in the following four specimens:

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Figure 6. Intramuscular nerve distribution of the obturator internus and gemelli muscles in man. Anterior views of the gemelli and the lateral view of the obturator internus. The branch to the quadratus femoris muscle is indicated by the black dot. A: Specimen 1 (right). B: Specimen 2 (left). C: Specimen 3 (left). D: Specimen 4 (right). IG, inferior gemellus muscle; OI, obturator internus muscle; Oi, obturator internus nerve; Qf, quadratus femoris nerve; SG, Superior gemellus muscle.

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  • Specimen 1 (right, Fig. 6A): The branches of the quadratus femoris nerve entered the anterior surface of the inferior gemellus and the infero-anterior part of the superior gemellus. Branches of the obturator internus nerve entered the posterior (or superficial) surface of the supero-posterior part of the superior gemellus.

  • Specimen 2 (left, Fig. 6B): The gemelli muscles were adjoined on the anterior surface of the obturator internus tendon. The branches to the superior gemellus from the communication between the obturator internus nerve and the quadratus femoris nerve were distributed to the posterior part of the superior gemellus, and to the superior part of the inferior gemellus. In addition, a twig of the communication joined with the branches to the inferior gemellus of the quadratus femoris nerve.

  • Specimen 3 (left, Fig. 6C): The branches to the superior gemellus originating from the quadratus femoris nerve and from the obturator internus nerve communicated with each other. The inferior gemellus was tightly adjoined with the inferiormost (or lowest) part of the obturator internus. A twig of the inferior gemellus branch extended within this fused region.

  • Specimen 4 (right, Fig. 6D): The superior and medial part of the inferior gemellus was tightly adjoined with the inferiormost part of the obturator internus. The inferior gemellus was innervated by branches of the quadratus femoris nerve from the anterior surface and by a branch of the obturator internus nerve from the superior surface. These branches communicated with each other. In this specimen, the superior and medial part of the inferior gemellus was additionally supplied by a branch of the obdurator internus nerve.

Rhesus Monkey

The terminology used here was mainly adopted after the text of Howell and Straus(1933).

The rotatory muscle group and its innervation.

The rotatory muscle group consisted of the gemelli, obturator internus, and quadratus femoris. The obturator internus originated from the inner surface of the pelvis, covered the obturator membrane, ran dorsolaterally, and inserted into the medial surface of the greater trochanter (Fig. 7). The caudal part of the muscle was much thicker than the cranial part. The superior and inferior portions of the gemelli muscles formed a continuous muscle sheet, known as “the gemellus pocket” ventral to the tendon (Fig. 8). The gemelli originated from the lateral surface of the ischial spine, which was proximal to the origin of the ischiocaudalis, from the dorsolateral border of the sciatic notch, and from the dorsomedial surface of the ischial tuberosity. The gemelli inserted into the medial surface of the great trochanter deep to the obturator internus tendon.

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Figure 7. Lateral view of the rotatory muscles and surrounding muscles in monkeys. The inferior gemellus originated from the medioposterior surface of the ischial tuberosity. F, femur; GI, inferior portion of gemelli muscles; GS, superior portion of gemelli muscles; IC, ischiocaudalis muscle; IL, ilium; IT, ischial tuberosity; OI, obturator internus muscle; P, piriformis muscle; QF, quadratus femoris muscle.

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Figure 8. An example of the obturator internus and gemelli muscles in a monkey. A: Posterior surfaces of the gemelli muscles and the medial surface of the obturator internus muscle. B: Anterior surfaces of the gemelli muscles and the lateral surface of the obturator internus muscle. G, gemelli muscles; GI, inferior portion of gemelli muscles; GS, superior portion of gemelli muscles; OI, obturator internus muscle.

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The gemelli and the quadratus femoris were innervated from the ventral surfaces by the quadratus femoris nerve. In two of eight specimens, the superior portion of the gemelli was also innervated by a branch of the obturator internus nerve from the dorsal surface. The obturator internus was innervated by the obturator internus nerve from the medial surface.

According to the findings of the intramuscular nerve distribution, the gemelli muscles were difficult to divide into the superior and inferior divisions. In the obturator internus muscle, the nerve branches were distributed anteriorly from the medial surface. Some branches, however, turned to distribute to the posterior (or superficial) and distal part of the muscle, which was very close to the inferior (or lower) division of the gemelli muscles (Fig. 4).

Composition and ramification of the main nerves of the sacral and pudendal plexuses.

A detailed description of the findings of Specimen 3 of the rhesus monkey (Specimen 3M) is given (left, Fig. 10). The common peroneal nerve was formed by the union of the dorsal trunks of L6 and L7. The ventral division of L6 and L7 as well as S1 united to form the tibial nerve. The femoral flexor nerve arose from the ventral surface of the union of L6 and L7 and S1, and ran along with the tibial nerve to innervate the flexor thigh muscles. The quadratus femoris nerve arose from the roots of the flexor femoral nerve of L6 and L7, whereas the obturator internus nerve arose from the roots of the flexor femoral nerve of L7 and S1. Therefore, the former seemed to be more cranial than the latter. The pudendal nerve was formed by the roots from the ventral surfaces of S1 and S2, and a branch, which originated from the ventral surface of the caudal-most root of the obturator internus nerve. The nerve to the iliopubocaudalis arose from the ventral surface of S2, whereas that to the ischiocaudalis arose from the dorsal surfaces of S1 and S2. Therefore, at the level of S1, the root of the pudendal nerve arose ventral to the root of the obturator internus nerve.

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Figure 9. Intramuscular nerve distribution of the obturator internus and the gemelli muscles in monkeys. Anterior views of the gemelli and the lateral view of the obturator internus. A branch to the quadratus femoris nerve is indicated by a black dot. A: Specimen 1M (left). B: Specimen 2M (right). G, gemelli muscles; OI, obturator internus muscle; Oi, obturator internus nerve; Qf, quadratus femoris nerve.

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In the other specimens, the segmental composition of the main nerves of the sacral plexus were almost similar to Specimen 3M. The quadratus femoris nerve arose from more cranial segments than the obturator internus nerve, however in two specimens the obturator internus nerve arose from the quadratus femoris nerve as a branch (Fig. 10). The pudendal nerve arose from more caudal segments than the obturator internus nerve. In addition, the pudendal nerve arose relatively ventral to the obturator internus nerve.

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Figure 10. Composition and ramification of the sacral and pudendal plexus in a monkey (ventral aspect). Specimen 3M (left). Fe, femoral nerve; Fx, femoral flexor nerve; Ig, inferior gluteal nerve; Ipc, nerve to iliopubocaudalis; Ic, nerve to ischiocaudalis; L, lumbar nerve; Ob, obturator nerve; Oi, obturator internus nerve; Pd, pudendal nerve; Per, common peroneal nerve; Pfc, posterior femoral cutaneous nerve; Qf, quadratus femoris nerve; S, sacral nerve; Sg, superior gluteal nerve; Tib, tibial nerve.

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DISCUSSION

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

According to the embryological studies reported by Gräfenberg (1904) and Bardeen (1907), the anlage of the obturator internus and gemelli, even from its earlier stages of differentiation, seems to be distinct from that of the quadratus femoris. In addition, when the obturator internus extends well over the obturator foramen and its nerve follows in the same direction, then the gemelli cannot be clearly distinguished from the obturator internus. According to the innervation findings, the gemelli are generally supplied by branches from the nerve to the quadratus femoris (quadratus femoris nerve), and these findings seem to suggest that the gemelli except for the part that is innervated by the nerve to the obturator internus (obturator internus nerve) have a close relationship with the quadratus femoris. The quadratus femoris is clearly distinguished from the other muscles based on the intramuscular nerve distribution findings. In the present study, a branch of the quadratus femoris nerve was also found to innervate the adductor magnus in two specimens, and this branch communicated with the obturator nerve. According to the fiber analyses of the lumbosacral plexuses, the cranial most root of the quadratus femoris nerve innervated the quadratus femoris muscle, and the root was closely related to the nerve to the adductor magnus from the obturator nerve. These findings confirm those of previous reports, including studies of marsupials (Wilson, 1888; Bardeen, 1907; Matsumura et al., 1986; Sakamoto et al., 1997). Interestingly in Thylacine and Cuscus, the adductor magnus is innervated by only the quadratus femoris nerve (Cunningham, 1881), and in some mammals the quadratus femoris is innervated by the obturator nerve instead of nerve from the sacral plexus (Bardeen, 1907). Therefore, it is suggested that the quadratus femoris is located in a critical position between the adductor muscle group and the obturator internus and gemelli muscle group. Although closely associated, it is suggested that the quadratus femoris is independent of the gemelli muscles as described by Gräfenberg (1904) and Bardeen (1907).

It has been already recognized that the obturator internus and gemelli muscles are divided from a single muscle anlage and are closely related to each other (e.g., Gräfenberg, 1904; Bardeen, 1907; Frohse and Fränkel, 1908; Braus and Elze, 1954). Recently, Shinohara (1995) and Honma et al. (1998) proposed recognition of the superior and inferior gemelli as different heads of the obturator internus based on the architecture of the muscles. In the present study, the origin of the inferior gemellus (or the inferior portion of the gemelli) was generally observed at the posteromedial surface of the ischial tuberosity, that is the intrapelvic region just beneath the lower margin of the obturator internus. It is well known that the gemelli may be absent, or fused with the obturator internus (e.g., Clemente, 1985; Bergman et al., 1988; Salmons, 1995). Miura (1932) reported the absence of the superior gemellus in both sides of a pair of twin fetuses. In most of the specimens of the present study in man, the gemelli were divided into the superior and inferior parts by their forms and muscle bundle directions, and in some specimens the border between the gemelli could not be clearly distinguished according to the intramuscular nerve distribution findings. In addition, in monkeys two portions of the gemelli form the gemellus pocket and are difficult to divide into two parts. The degree of isolation of the gemelli and their manner of attachment to the obturator internus vary as described by Bardeen (1907) based on findings in different mammals. It is obvious, however, that the obturator internus and the gemelli are closely related.

The superior gemellus is frequently innervated by both the quadratus femoris nerve and the obturator internus nerve. The frequency of dual nerve supply to the superior gemellus is varied: 20.0% (Kikuchi, 1987b), 29.4% (Honma et al., 1998), 60.4% (present study), 86% (Shinohara, 1995). Kikuchi (1987b) recognized the superior gemellus as a muscle of dual innervation, and described that the quadratus femoris nerve and the obturator internus nerve are completely different nerves based on their different courses and the lack of communication between the nerves. It has been proposed that two compartments that have different nerve supply fuse together and form a muscle of dual innervation, and the region of dual innervation of the muscle appears at the transitional zone of two ontogenetically different muscular masses (Paterson, 1894; Last, 1949; Takahashi, 1982). According to the findings of the segmental composition, the quadratus femoris nerve is thought to originate from more cranial segments than the obturator internus nerve, although some segments overlap. In the present study, the quadratus femoris nerve and the obturator internus nerve frequently communicated both within and outside the muscles in various patterns. In monkeys, these nerves sometimes originated as a common trunk. Because the quadratus femoris nerve and the obturator internus nerve are not clearly distinguished from each other, it is difficult to recognize the superior gemellus as a true muscle of dual innervation. The obturator internus and the inferior gemellus are sometimes innervated by both nerves. These muscles are located between the obturator internus nerve and the quadratus femoris nerve, therefore, they could be innervated by both nerves. The quadratus femoris is clearly independent from the obturator internus and gemelli, and the nerve, which innervates the quadratus femoris, seems to be an independent nerve, although it is not clearly distinguished from the nerves to the gemelli. It may be concluded that the nerves to gemelli that run deep to the gemelli and the nerve innervating the quadratus femoris might secondarily unite to form the quadratus femoris nerve.

The obturator internus nerve has various origins that are widely spread segmentally from the sacral plexus and the pudendal plexus. Kikuchi (1987a,b) classified the obturator internus nerve into three types according to its relationships with the roots of the pudendal nerve and sciatic nerve: 1.) sciatic nerve type, 2.) transitional type, and 3.) pudendal nerve type. In dogs, cats, rabbits and rats, the most frequent type is the pudendal nerve type, and in guinea pigs, the transitional type (Kikuchi, 1987a). In man, however, the sciatic nerve type is the most frequent type (Kikuchi, 1987b). According to comparative anatomical studies (Akita, 1992a,b, 1997; Akita et al., 1992, 1995), the craniocaudal and dorsoventral relationships between the pudendal nerve and the nerve to the muscle homologous to the obturator internus are constant in various species. Although it is very difficult to analyze the dorsoventral relationships of the main nerves of the sacral plexus with the pudendal nerve in man, the pudendal nerve is situated ventral to the obturator internus nerve in various species (Akita and Yamamoto, 1995; Akita et al., 1995). Therefore, the obturator internus nerve is located in the craniocaudal and dorsoventral intermediate zone between the sacral plexus and the pudendal nerve. The quadratus femoris muscle is an extrapelvic muscle, whereas the muscles innervated by the pudendal nerve are intrapelvic muscles. The obturator internus extends and spreads from the extrapelvic to intrapelvic regions, and is considered as an intermediate transitional muscle between the extrapelvic and intrapelvic muscles (Table 4). Taken together, it is suggested that the more ventrocaudal part of the anlage of the ventral muscle group tends to migrate to the intrapelvic space.

Table 4. Topographical nerve relationships as a basis for muscle orientation
 Nerve originMuscles supplied
Sacral plexusDorsalCranialExtrapelvic
Quadratus femoris nerve (Qf)IntermediateIntermediate (more cranial than Oi)Extrapelvic
Obturator internus nerve (Oi)IntermediateIntermediate (more caudal than Qf)Extra- and intrapelvic
Pudendal nerveVentralCaudalIntrapelvic

Based on our findings and embryological findings reported by Bardeen (1907), we propose a model which explains the close relationships among the gemelli and obturator internus (Fig. 12). Because the findings in monkeys are basically similar to those in humans, our model is based primarily on humans. The muscle anlage of the obturator internus is thought to move anteromedialward in the developmental stage. We suggest that during this migration the muscle bundles extend medial to the ramus of the ischium (intrapelvicward) form the obturator internus, and those that remain lateral to the ramus form the gemelli. The variations in the patterns and routes of the innervating nerves reflect the variability of the differentiation patterns of the anlage.

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Figure 11. Posterior view of the gemelli and obturator internus in a monkey. Specimen 4M (right). The quadratus femoris nerve and the obturator internus nerve formed a common trunk (indicated by a star). A branch indicated by black paper is a branch to the superior portion of the gemelli from the obturator internus nerve. GI, inferior portion of gemelli muscles; GS, superior portion of gemelli muscles; IC, ischiocaudalis muscle; IT, ischial tuberosity; OI, obturator internus muscle; Oi, obturator internus nerve; Pd, pudendal nerve; QF, quadratus femoris muscle; Qf, quadratus femoris nerve; Sc, sciatic nerve.

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Figure 12. Schema of a possible model of the developmental formation of the obturator internus and gemelli muscles based on the embryological study of Bardeen (1907) as well as the present innervation findings. A: Initial stage. The anlage of the obturator internus (obturator internus anlage) that includes the anlage of the gemelli seems to be distinct from the anlage of the quadratus femoris (quadratus femoris anlage). The quadratus femoris anlage is directly supplied by a nerve from the sacral plexus in this stage. The obturator internus anlage migrates intrapelvicward. The obturator internus anlage is theoretically divided into the areas that are innervated by the obturator internus nerve from the posterior surface and innervated by the nerve from the anterior surface. B: Definitive stage. The positional relationship between the obturator internus, gemelli and quadratus femoris muscles and their innervating nerves is shown. The nerve to the quadratus femoris anlage runs along the nerve to the obturator internus anlage that innervates the anlage from the anterior surface. Therefore the quadratus femoris nerve might consist of two nerves. The quadratus femoris nerve also innervated the adductor magnus in some cases. The quadratus femoris nerve and the obturator internus nerve communicate inside and outside the gemelli and obturator internus muscles. The superior gemellus ceases to migrate to the intrapelvic space due to the presence of the ischiadic spine, but the inferior gemellus often originates from the medial surface of the ischiadic tuberosity. Am, branch to adductor magnus; IG, inferior gemellus muscle; IS, ischial spine; IT, ischial tuberosity; OIA, anlage of obturator internus; OI, obturator internus muscle; Oi, obturator internus nerve; Oia, nerve to obturator internus anlage; QFA, anlage of quadratus femoris muscle; QF, quadratus femoris muscle; Qf, quadratus femoris nerve; Qfa, nerve to quadratus femoris anlage; SG, superior gemellus muscle.

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Acknowledgements

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED

We express our thanks to Ms. Kamei for her drawing advice and kind assistance for this study.

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. LITERATURE CITED
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