Intrinsic Hand Muscles of Primates with
Special Reference to Human Trisomy Syndromes

Samuel Strong Dunlap, Ph.D. Reston, Virginia and M.A. Aziz, Ph.D. Howard University College of Medicine Washington, D.C.

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: hand muscles, ontogeny, Primates, human trisomy, atavism.

© copyright 2012 Samuel Strong Dunlap, Ph.D.

ABSTRACT

Descriptions of intrinsic thenar and contiguous hand musculature are equivocal regarding their actual complexity. Frequently, there is difficulty in differentiating the two independently innervated heads of the flexor pollicis brevis. Similarly, the deep head (of Cruveilhier) of the flexor pollicis brevis is frequently confused with the interosseous palmaris I of Henle (i.e. “the 1st palmar interosseous”), a distinctly separate volar muscle located in the vicinity of the thumb. Comprehensive analysis based on dissections of several nonhuman primates as well as normal and karyotypically anomalous (aneuploid/trisomic) humans leads to a clarification of the identity of thenar and related muscles. Decelerated myogenesis associated with human trisomic phenotypes assists in a clearer definition of the controversial muscles based on knowledge of their embryogenesis. Developmental myological retardation of human trisomic phenotypes also leads to the retention of those ulnarward contrahentes, which are normally absorbed during embryogenesis. Contrahentes ontogeny clarifies the status of the extant human adductor pollicis. The molecular, cytogenetic and evolutionary bases of these phenomena are discussed.

INTRODUCTION

Comparative myology constitutes a significant avenue elucidating primate phylogeny and systematics (St. John Brooks, 1886a & b ; McMurrich, 1903; Howell & Straus, 1933; Loth, 1931; Howell, 1936; Straus, 1941, 1942, 1946a, 1946b; Washburn, 1950; Day & Napier, 1963; Napier, 1964, 1967; Ashton & Oxnard, 1963 ; Stern, 1971; George, 1977; Stern et al., 1977; Stern & Susman, 1981; Tuttle, 1981; Aziz & Dunlap, 1986; Dunlap et al., 1985). Especially noteworthy are limb muscle comparisons predicated on the dramatic morphological and functional changes engendered by erect bipedalism and forelimb prehension amongst hominoids (Napier, 1962, 1964, 1967). Since obligatory power- and (especially) precision-grip are the hallmark of hominoid evolution, considerable research interest has been directed at the comparative myology, the evolution, and the morphology of primate hands, the thumb especially (McMurrich, 1903; Day & Napier, 1961, 1963; Napier, 1956, 1961, 1976; Tuttle, 1969a, 1969b, 1981; Aziz & Dunlap, 1986). However, despite numerous elucidative works, there remain significant discrepancies in data and interpretations based on them. To some extent, these inconsistencies are caused by incomplete, insufficient or conflicting reports on the occurrence, incidence and variation of muscles and associated structures.

In an attempt to expand and re-evaluate data on cheiridial musculature, we have reported on dissections of numerous primate genera, including humans (Aziz & Dunlap, 1986; Dunlap & Aziz, 1985: Dunlap et el., 1985). However, these studies have largely focused on extrinsic hand muscles. The present investigation centers on intrinsic manual muscles, especially those of the thenar region, whose evolution critically facilitated the origin and refinement of the precision grip, a prerequisite of habitual tool use and manufacture (Napier, 1967; Aziz & Dunlap , 1986; Marzke & Shackley, l986)
Impetus for these investigations is mainly based on the discovery of several supernumerary muscles which, although sporadic and infrequent amongst normal humans, occur with high frequency amongst human fetuses and neonates trisomic for chromosome numbers 13, 18 and 21 (Macalister, 1875; Pettersen & Bersu, 1982; Dunlap et al., 1986). Several such muscles are reminiscent of those found in earlier primate taxa. Barash et al. (1970) considered them “atavistic”, i.e, muscles which repeat themselves “in successive ontogenies” (deBeer, 1958). Further observations based on numerous comparative myological analyses of adult and neonatal monkeys, apes and humans considerably bolstered Barash et al.’s (1970) tentative phylogenetic assessment of atavistic musculature (Aziz, 1981a; Dunlap et al., 1985). However, neither Barash et al., (1970) nor Aziz (1981a) had a comprehensive explanation of muscle atavisms associated with human trisomies, although the platysma occipitalis, an unusual facial muscle common amongst trisomic neonates, looked identical to that recorded by Gasser (1967) in normal human fetuses (Bersu & Ramirez-Castro, 1977; Aziz, 1981a, 1981b). Significantly, the platysma occipitalis is a well-developed muscle in many adult nonhuman primates (Huber, 1930; Howell & Straus, 1933). Its occurrence suggested the likely presence of other transient embryonic and/or fetal atavistic muscles in normal humans (Aziz, 1981b).
Unbeknownst to Aziz (1981a) were earlier osteomyological investigations of staged, normal human embryos and fetuses by Cihak ( 1972, 1977) and Dylevski (1967, 1968) recording their unequivocal, albeit transitory existence. The latter work led Aziz & Dunlap (1986 ) and Dunlap et al. (1986) to argue that frequent presence of atavistic muscles in human trisomic infants is due to arrested or delayed development characteristic of human aneuploidy (Hall, 1965; Shapiro, 1975, 1983, 1989). The preservation at perinatal age, of several embryonic/fetal supernumerary muscles in human trisomy provides readily-appreciated examples of otherwise obscure, ephemeral and routinely-neglected though phylogenetically significant phases of early ontogeny. By delaying development, aneuploidy retains transient embryonic myology and magnifies morphogenesis, facilitating investigative scrutiny.

Comparative studies of normal human embryos and fetuses (Cihak, 1972, 1977; Dylevski, 1967, 1968) and aneuploid phenotypes (Barash et al., 1970; Opitz et al.,1979; Aziz, 1981b; Pettersen & Bersu, 1982 ) have revealed pertinent previously unavailable data regarding the evolutionary relationships of primates. Further, the neuromuscular specificity of each trisomy syndrome contributes to our knowledge of how normal development occurs, what information may be present on effected chromosomes, the embryological origin of muscles, and evidence of the relationship between ontogeny and phylogeny (Pettersen & Bersu, 1982; Dunlap et al., 1986). Musculature discussed in this paper does not, of itself, constitute a sufficient number of characters upon which evolutionary classification can be advanced (Simpson, 1961; Mayr, 1969, 1981). However, as we have employed these and other muscle characters in our analyses of platyrrhine (Dunlap et al., 1985) and hominoid (Dunlap & Aziz , 1985) relationships, further discussion of their homology and polarity is relevant. Intrinsic hand musculature is probably the most primitive of tetrapod forelimb musculature (Miner, 1924; Bunnell, 1944), Some extrinsic hand musculature in higher tetrapods is derived from intrinsic hand muscles such as extensor digitorum profundus (Straus, 1941; Aziz &Dunlap, 1986) and flexor digitorum sublimis (Dylevski, 1968).

For this report we have compared and contrasted selected intrinsic hand muscles—especially the ulnar head of flexor pollicis brevis ( hereafter the “deep head of Cruveilhier”), the interosseous palmaris I of Henle, the opponens pollicis and the contrahentes of nonhuman primates, aneuploid humans and normal humans of various ages in order to: 1) reinterpret and clarify extant data, 2) assess the functional and evolutionary changes in normal musculature in light of changing patterns of selection and 3) to reassert the significance of ontogeny in ushering morphological novelty which, in turn, spurs evolutionary change (Hardy, 1963).

MATERIALS AND METHODS

Human aneuploid fetuses and neonates (Table 1) used in this study include five trisomy 13, ten trisomy 18, and two trisomy 21 cases (including a confirmed trisomy 21 fetus, and an unkaryotyped adult whose clinical history was consistent with trisomy 21). The latter case is included with the same reservation attending a similar case of trisomy 13 in a paper by Pettersen et al., (1979).
Also dissected were hands of the following (Table 2 ) platyrrhine monkeys: five Cebus apella (USNM 398912, 497821, 535008, 535010, 535011), four Saimiri sciureus (USNM` 395650, 395657, 497092, 502645), one Aotus sp. (USNM 497019), one Callicebus moloch (USNM 484997), one Callimico goeldii (USNM 535014, two Callithrix argentata (USNM 535238, 525241), one Callithrix jacchus (USNM 536844), one Saguinus geoffroyi (USNM 497216), one Saginus mystax (USNM 395973), one Leontopithecus rosalia (USNM 380472), one Cebuella pygmaea (USNM 399610), one Lagothrix lagotricha (USNM 398029), two Ateles geoffroyi (USNM 399104, 502456), and one Alouatta palliata (USNM 543125); and the following Catarrhine monkeys: two Macaca nemestrina (HU 301, 302), one Cercopithecus talapoin (USN 395447), one Cercopithecus aethiops (USNM 398006),one Hylobates syndactylus (USNM 3973394), one Hylobates lar (HU 351), one Gorilla gorilla (HU 349), one Pan troglodytes (HU 350), one Pongo pygmaeus (HU 348), and one Galago crassicaudatus (USNM 397997).

All specimens were adult except one Cebus and the Hylobates syndactylus which were juveniles; the great apes were neonatal. Our observations were based on gross dissections done primarily with a dissecting microscope following the protocol outlined in Cunningham’s Manual of practical Anatomy (Romanes, 1966). Iodine solution was frequently employed as a stain (Bock and Shear, 1972) to distinguish muscular fibers from connective tissue, particularly in the fetal material.

The terminology follows Howell and Straus (1933), Mortensen and Petterson (1966) and Goss (1973). A written record of our dissections, including black and white, and color photographs, as well as drawings, were kept. Roentgenograms of the hands were used for drawings and to determine topographic relations. Quantifiable data is tabulated. Table 1 facilitates easy comparison with Dunlap et al.(1986), and other trisomy neuromuscular publications. Table 2 facilitates comparison with Day and Napier (1963). Since our limited sample size did not permit inference of randomness, more sophisticated statistical procedures were not applied. Nerve supply of muscles is omitted except where relevant to establishing homology. More complete clinical information on trisomies and their forelimb musculature and that of our primates may be found in our publications (Aziz and Dunlap, 1986; Dunlap and Aziz, 1985; Dunlap et al., 1986).

Detailed descriptions of hand muscles exhibiting unusual or heretofore unreported variations only appear below. These include muscles of the thenar compartment and the contrahentes muscles. One specimen of trisomy 18 (Case 2), regrettably returned before deep hand dissection could be completed, is not described with reference to the deep hand muscles.

RESULTS

Flexor pollicis brevis (superficial head)
Nonhuman primates did not exhibit anything remarkable about this superficial head of the flexor pollicis brevis except Ateles, in which it was diminutive. This muscle head was absent in only a few human trisomy hands, usually in conjunction with abductor pollicis brevis. It was occasionally fused with opponens pollicis in trisomy 18.

Deep head of Cruveilhier
No platyrrhine exhibited the deep head of Cruveilhier. Amongst Old World primates only Macaca and Cercopithecus possessed it. The muscle was present in only three trisomy 13 hands, six trisomy 18 hands and both trisomy 21 cases. These were very similar to the most frequent manifestation of the deep head of Cruveilhier reported by Day and Napier (1961), in which insertion was radialward with the flexor pollicis brevis (superficial head) in 53 of 65 hands of dissecting-room (presumably karyotypically normal) cadavers.
Interossesous palmaris I of Henle
The interosseous palmaris I of Henle ( Robinson, 1931; Wood Jones, 1942; Breathnach, 1965; Lewis, 1965) was only seen in Cebus apella amongst platyrrhines. It was well-developed in Macaca and was present in all apes (Figure 1). It was absent in Cercopithecus and Galago
In Cebus the muscle differed in origin from all other nonhuman primates and most human aneuploids. It originated from the radial side of the carpal tunnel, i.e., just superficial to its normal site of origin in other species, including karyotypically normal humans. In other respects the muscle was as encountered in other primates; it was distinct from opponens pollicis, inserting with contrahens I (adductor pollicis) on the ulnar side of the base of the proximal phalanx of the first digit. In Cebus the muscle could also be described as an ulnar head of flexor pollicis brevis. We have encountered an identical configuration in two trisomy 18 cases (5 and 9, bilaterally).

Figure 1

legend figure 1

 

In Pan (Figure 1) the interosseous palmaris I of Henle was very small, originating from the base of metacarpal I; it was proximally tendinous, and distally muscular. It was separated from the opponens pollicis and other deep muscles. The insertion was on the volar surface of the first metacarpophalangeal joint, between insertions of contrahens I and flexor pollicis brevis, both of whose insertions extended volarward. The long flexor tendon to the thumb was lacking. In Gorilla (Figure 1)the interosseous palmaris I of Henle was a fibrous sheet originating from the ulnar margin of metacarpal I and separate from opponens pollicis and the other deep muscles. The sheet formed a tendon which inserted on the distal phalanx of the thumb. Again, there was no pollical flexor tendon. In Pongo (Figure 1) the muscle originated normally from the ulnar margin of metacarpal I, was distinct from adjacent muscles, and inserted normally. Significantly, the long flexor was also absent in Pongo. However, a small tendon to the distal phalanx of the thumb originated from the insertion of the robust contrahens I. Although the interosseous palmaris I of Henle inserted with the contrahens I on the ulnarward base of the proximal phalanx, there was no direct contribution to the tendon which inserted on the distal phalanx. In Hylobates the interosseous palmaris I of Henle was present along with the flexor pollicis longus, albiet the latter was diminutive in both species.

The interosseous palmaris I of Henle was absent in one trisomy 13 and three trisomy 18 hands, respectively. In trisomy 13 (Case 4), on the right side, the interosseous was represented by a thin sheet of muscle lying adjacent to the ulnar side of metacarpal I. Unusual configurations of this muscle were found in other trisomy hands as well. In one trisomy 13 (Case 2, left) the muscle belly was tendinous proximally and gave way to a distal venter before inserting with contrahens I, this resembled Pan. In trisomy 18 (Case 3, left) flexor pollicis brevis superficialis was so diminutive that insertion was almost entirely on the ulnar side of the first proximal phalanx base. Since a portion of the origin was from the ulnar margin of the proximal metacarpal I, the muscle was indistinguishable from the interosseous palmaris I of Henle. Figure 2 illustrates interosseous palmaris I of Henle in Case 3 on the right.

Opponens pollicis
Amoungst platyrrhines, the opponens pollicis had a radialward insertion along most of metacarpal I, except in Callimico, Saguinus, Callithrix, and Cebuella where insertion was confined to its proximal end. The muscle was absent in Leontopithecus. All catarrhines had well-developed opponens pollicis inserting on the radial side of metacarpal I. Opponens pollicis was present in all trisomy hands; it was diminutive in only five hands. In the left hand of trisomy 13 (Case 5), it originated from the first carpometacarpal joint and the proximal shaft of metacarpal I and inserted on the volar surface of metacarpal I rather than the preaxial side of the shaft . At its origin the muscle was continuous with the interosseous palmaris I of Henle. Innervation was by a terminal branch of the ulnar profundus nerve. The other four diminutive opponens were in trisomy 18 hands. Case 3 exhibited a thin, aponeurotic muscle with a proximal insertion on the radial side of the metacarpal I shaft (Figure 2). In Case 6, on the right, the muscle was represented by a radialward expansion of the interosseous palmaris I of Henle which inserted on metacarpal I.

figure 2

legend figure 2

The contrahentes muscles
These four adductors, lying superficial to the interossei, are found in most primates, and amongst many other mammalian taxa. In most groups they originate from the mid-distal carpal bones, their associated ligaments, and a median raphe along the volar surface of metacarpal III shaft (Young, 1880; Howell and Straus, 1933; Haines, 1955; Dunlap et al., 1985). The ulnarward contrahentes are absent or diminutive in most apes. Post-fetal humans have lost all contrahentes except the first, i.e. adductor pollicis. Occasional contrahentes II, IV and/or V were recorded in five trisomy 18 hands. No contrahentes other than the adductor pollicis appeared in other trisomies. When present, the contrahentes were frequently diminutive; however, they all originated from the median raphe or mid-distal carpal bones. Several were appreciably large and were unequivocally located superior to the ulnar profundus nerve, an important criterion for muscle identification and for establishing myological homology (Howell and Straus, 1933).
With the exception of the absence of contrahens IV in Ateles, Lagothrix and Alouatta, a full set of contrahentes (I, II. IV and V) was found in platyrrhines. This was also the case in Galago, Macaca and Cercopithecus. In Galago, the origin of contrahens I extended from the median raphe to the deep transverse metacarpal ligament between digits II and III (Hollinshead, 1969; Goss, 1973). Pan had contrahentes I, IV and V (Figure 1). In Pongo, there was a separate slip of muscle originating from the radial side of the proximal phalanx II base near the insertion of the first lumbrical which fused at its insertion with contrahens I. The contrahentes were quite different between the two Hylobates specimens. The juvenile specimen from the Smithsonian collection possessed a full set of contrahentes albiet quite reduced compared to Macaca or many other mammals. In particular, contrahens I originates from the median raphe which only extends half-way down the shaft of metacarpal III so the transverse head is absent. Additionally, there is an ulnarward radiation of the raphe from which much of contrahens IV and V arise. The adult specimen of Hylobates lar in our lab has only the contrahentes I of unusual morphology : a. the transverse and oblique heads are poorly separable, b. the transverse head has an extensive origin from a median raphe running the length of metacarpal III, from another raphe-like aponeurosis off the intermuscular fascia between the two palmer interossei of metacarpal IIII and that bone, c. the transverse head originates also from the distal transverse metacarpal ligaments between II, III,and IIII, d. and finally, that portion of the transverse head originating from metacarpal IIII forms a poorly separating sheet of muscle superficial to a deeper portion of the transverse head originating from metacarpal III and the distal transverse metacarpal ligaments mentioned above. Hartman & Straus (1933) mention an oblique extension of the median raphe onto the fourth metacarpal in their discussion of the median raphe in Macaca.

The contrahentes in human trisomies

Contrahens I (adductor pollicis) was universally present in trisomy hands. Absence of its transverse head was noted in trisomy 18 (case 4). A separate slip, as described in Pongo, was also encountered in seven trisomy 18 hands; earlier, we had provisionally designated it as a lumbrical occurring between digits I and II (Dunlap et al., 1986). In all cases the slip was too diminutive to permit identification of nerve supply. In trisomy 18 hands the slip also did not share the close morphological relationship with contrahens I as in Pongo, The transverse head of adductor pollicis did not originate as far ulnarward in trisomy 18 hands as it did in Pongo.

Contrahens II was found in six trisomy 18 hands, bilaterally in Cases 3 and 4 and on the left in cases 1 and 5. In the unilateral cases the muscle was just a tiny slip, originating from the distal portion of the median raphe, lying deep to the transverse head of adductor pollicis, separate from the deeper interossei, and inserting with the second palmar interosseous on the base of the proximal phalanx of digit II. The bilateral occurrence of contrahens II in case 3, although diminutive compared to most monkey hands, was the best representation of this muscle in human trisomies (Figure 2). On both sides it existed as two slips originating from the median raphe, The right hand is illustrated in Figure 2, and the left, in a similar illustration, may be seen in Dunlap et al., (1986). The proximal slip originated superficially to the ulnar profundus nerve which passed deep to contrahens I and through the median raphe. The other case was less developed.

Contrahens IIII was found in the left hand of trisomy 18, Case 4. This tiny slip originated from the distal portion of the median raphe and inserted on the radial side of the metacarpophalangeal joint of digit IIII.

Contrahens V was found twice in trisomy 18 hands: on the right in Case 3 (Figure 2), and on the left in Case 10. In both the muscle originated from the ligament over the mid-distal carpals and the base of the metacarpal IIII, passed superficially to the ulnar profundus nerve, and inserted on the radial side of the proximal phalanx of digit V.

DISCUSSION OF MYOLOGY

Thenar muscles
Cihak (1969, 1972) has demonstrated that the human flexor pollicis brevis (the superficial head and the deep head of Cruveilhier), opponens pollicis, interosseous palmaris I of Henle, and the radial contribution to the first dorsal interosseous muscle are derived from a single embryonic blastema. From its inception, this blastema is separate from the more superficial and radialward blastema of abductor pollicis brevis and the blastema of the more superficial and ulnarward contrahentes. The entire interosseous blastema passes briefly through stages of development reminiscent of the interossei in mammals, including primates (Cihak, 1960, 1963, 1972, 1977). Therefore, embryological evidence, an important criterion for establishing homologies (DeBeer, 1958), indicates that the interossei are most likely homologous to the ancestral digital flexores breves profundi of mammals (Cihak, 1960, 1963; Lewis, 1965). The opponens pollicis and the interosseous palmaris I of Henle represent the flexors breves profundi of the thumb.

Despite pronounced developmental retardation characteristic of most aneuploid organ systems, the opponens pollicis was well-developed in nearly all trisomy hands. Although Cihak (1969) is not explicit regarding the morphology of the early differentiating opponens pollicis, the blastema apparently extends the full length of metacarpal I. This probably reflects the primitive condition of this muscle. Even when the opponens pollicis was diminutive in trisomy hands (Table I), in two instances only was insertion confined to the proximal end of the shaft (trisomy 18, Case 3 and 10; right hands). According to Cihak (1969), in the human adult, the origin of the opponens pollicis and flexor pollicis brevis superficialis results from a superficial migration of the origin from metacarpal I to the ligamentous flexor retinaculum, This is probably the case in most primates since the adult origin of these muscles is primarily from the flexor retinaculum (Howell and Straus, 1933).

The interosseous palmaris I of Henle has been retained in only a few primates examined in our study. Amongst platyrrhines, only Cebus apella exhibits this muscle. However, its origin too has migrated off the floor onto the ligamentous distal margin of the carpal tunnel. Dunlap et al. (1985) state that, in Cebus, this muscle is clearly distinguishable from the radial margin of contrahens I; thus, it is distinct from the deep head of Cruveilhier (Day and Napier, 1961). Three hands in trisomy 18 (Cases 5 and 9) exhibited migrated examples of this muscle. The origin of the muscle in these hands is clearly from the superficial distal ligamentous margin of the carpal tunnel; and, again, it is distinct from the contrahens I. All ape specimens exhibited interosseous palmaris I of Henle.

The unusual tendons to the distal phalanx of the thumb in Pongo and Gorilla suggest that tendon development may be autonomous as indicated by the absence of flexor pollicis longus in these two specimens. By our definition the flexor pollicis longus is the separate muscle and tendon derived from the deep layer of the forearm flexors normally found in humans. Although most of our specimens exhibited flexor digitorum profundus as described earlier (Windle, 1890; Hepburn, 1892; Howell and Straus, 1933; Straus, 1942; Jouffroy, 1962; Dunlap et al., 1986), very few possessed flexor pollicis longus and flexor digitorum profundus. In Gorilla, Raven (1950, p.45) reported a flexor pollicis longus with an “extremely delicate” tendon of insertion, which “ ... runs between the short flexors of the pollex , ...”. Short tendons similar to those found in our specimens have also been observed in apes by Day and Napier (1963) and by Tuttle (1969, 1970). Neither study attributes these tendons to the derivatives of the flexor pollicis longus tendon whose venter is usually lacking in apes, particularly in Pongo (Tuttle, 1970). Our Pongo showed no flexor pollicis longus nor any contribution from flexor digitorum profundus to the thumb (Dunlap and Aziz, 1985), It is probable that these little tendons are derived from tendons associated with the flexor pollicis longus.

Studies of vertebrate limb development (Chevallier et al., 1977; Hinchliffe and Johnson, 1980; Wachtler et al., 1982), experimental and observational reports of limb malformations (Shellswell, 1977; Bogusch, 1980; Bonner, 1980; Lewis et al., 1981; Stephens et al., 1982; Fallon & Caplan, 1983; Kieny et al., 1983; Mauger et al., 1983; Stephens and Strecker, 1983; Strecker and Stephens, 1983), and our studies of human aneuploids (Dunlap et al., 1986) indicate that bone, tendon, loose connective tissue, muscle, and nerves develop with significant autonomy. Thus, it is not unreasonable to expect a tendon to acquire a new muscle attachment on the preaxial forelimb under altered selective pressures.

The incidence of the deep head of Cruveilhier in trisomies (possibly excepting Down Syndrome) is much lower than in normal humans, probably due to delayed development. This muscle may be an independently derived character in Old World monkeys and in humans; the muscle was absent in apes. Day and Napier (1963) reported it in Pongo pygmaeus only. Alternatively, its presence in some catarrhines may suggest its occurrence amongst ancestral anthropoids. Presumably, its disappearance in apes is associated with the progressive reduction of the pollex.

Day and Napier (1961) reported 53 of 65 human hands which had a radialward insertion of the deep head of Cruveilhier, and 8 of 65 having dual insertions. However, this muscle, normally occurring with radialward insertion, originated from the floor of the carpal tunnel in very close association with contrahens I. We emphasize that this muscle is distinct and not to be confused with interosseous palmaris I of Henle.

We have examined twenty-eight human anatomy texts , two 19th century anatomical models, and all of the 40+ antebrachial and/or hand wax models on display in La Specola museum in Florence, Italy in order to ascertain the status of deep thenar musculature . Not surprisingly, these books ( Gerrish, 1902; Dwight et al., 1906; Bryce, 1923; Huber, 1930; Robinson, 1931; Grant, 1942; Jamieson, 1946; Anson, 1950; Lockhart et al., 1959; Zuckerman, 1961; Breathnach, 1965; Grant and Basmajian,1965; Mortensen and Pettersen, 1966; Romanes, 1966; Hollinshead, 1969; Grant, 1972; Goss, 1973; Warwick and Williams, 1973; Woodburn, 1973; Gardner, Gray and O’Rahilly, 1975; McMinn and Hutchings, 1977; Tobias and Arnold, 1977; Anderson, 1978; Ferner, 1980; Romanes, 1981; Snell, 1981; Cartmill et al., 1987; Stern, 1988) and models (Worden, 1988) present various interpretations of interosseous palmaris I of Henle and of the deep head of Cruveilhier. Neither 19th century model exhibits the interosseous palmaris I of Henle. The wax model from the University of Szeged, Hungary, only shows the other interossei. The other model, an Auzoux papier mache of the hand with removable parts, shows the deep head of Cruveilhier originating from the deep, distal carpal retinaculum and tunnel, passing deep to the tendon of flexor pollicis longus. Because the model has shrunk, insertions are no longer clearly delineated. Otherwise, it is in accord with descriptions in French textbooks (Day and Napier, 1961). No wax anatomical models on display in the La Specola museum in Florence show the interosseous palmaris I of Henle. As embryological studies of Cihak and associates become more generally known, confusion regarding the correct identity of these muscles will diminish.

Cihak (1969) reported that the deep ulnarward elements of the differentiating thenar blastema (the deep head of Cruveilhier, the interosseous palmaris I of Henle, and the radial contribution to the first dorsal interosseous) are innervated, as in the normal adult, by the ulnar profundus nerve. The variably reported presence of interosseous palmaris I of Henle , the deep head of Cruveilhier, (which is usually innervated by the ulnar profundus nerve), and the morphological confusion between these two muscles in adults have led to various explanations in the literature. On functional, morphological, and phylogenetic grounds, Day and Napier (1961) argue that the deep head of Cruveilhier is a “…part of the flexor pollicis brevis muscle, ...” (p.129), however, “part of” is not the same as “being derived from”. Earlier they wrote that “ ... the close relation of the deep head at its origin to the oblique head of adductor pollicis makes it likely that it is a derivative of the contrahentes layer of the mammalian intrinsic palmar musculature ( St. John Brooks, 1886a & b; McMurrich, 1903; Haines, 1935) from which the adductor pollicis of man has been derived.” Further, on the basis of thenar muscle dissections of 36 primate species they state that “… the deep head of flexor pollicis brevis in man is derived from the contrahentes layer…” (Day and Napir, 1963, p.132). Since their study did not include interosseous palmaris I of Henle, information on the incidence and variation of this muscle is not yet satisfactorily established, In thirteen of the twenty eight textbooks we studied, the interosseous palmaris I of Henle was clearly recognized as a separate muscle occurring deep to the deep head of Cruveilhier (Bryce,1923; Huber, 1930; Robinson, 1931; Grant, 1942; Jamieson, 1946; Lockhart et al., 1959; Zuckerman, 1961; Breathnach, 1965; Mortensen and Pettersen, 1966; Warwick and Williams, 1973; Gardner et al., 1975; Tobias and Arnold, 1977; Cartmill et al., 1987). In four of the remaining fifteen texts confusion regarding the identity of the interosseous palmaris I of Henle and the deep head of Cruveilhier is discussed (Dwight et al., 1906; Hollinshead, 1960; Goss, 1973; Snell, 1981).
The incidence of the interosseous palmaris I of Henle is not reported in any recent textbook. However, Warwick and Williams (1973) state that there is no gross variation of the interossei in humans. Wood Jones (1942) indicates the presence of four palmar interossei in humans, the first clearly being interosseous palmaris I of Henle. Cihak (1972) states that this muscle is variable in humans. Abramowitz (1955) and Lewis (1965) reported the interosseous palmaris I of Henle in all the human hands they studied. Judging by their detailed descriptions, it appears likely that neither Abramowitz (1955), Day and Napier (1961) nor Lewis (1965) failed to correctly identify these muscles. Nevertheless, unequivocal identification requires an anatomical study involving the simultaneous examination of all thenar, radialward interossei and contrahentes muscles; this is necessary because confusion continues to exist regarding the incidence and variation of the deep thenar musculature. We have begun such a study. To date, our sample of thirty hands exhibit both the deep head of Cruveilhier in all cases and the interosseous palmaris I of Henle, in all cases. In eleven of 30 hands the deep head of Cruveilhier and the contrahens I (adductor pollicis) present a nearly continuous insertion across the volar surface of the distal metacarpal shaft deep to the flexor pollicis longus tendon. Not surprisingly, the interosseous palmaris I of Henle manifests considerable morphological variation upon which we are preparing a separate publication with a review of the literature.

The contrahentes
Cihak (1972) states that muscle strips, which may represent ulnarward contrahentes are frequently found in adult humans. However, in the absence of anatomically correct insertion and an origin superficial to the ulnar profundus nerve, they may be slips of unknown origin, Published literature provides no convincing account of ulnarward contrahentes in humans. Flower and Murie’s (1867) dissection of a Bushwoman includes a hand muscle originating from the “process of the unciform bone” which lay superficial to the opponens digiti minimi, suggesting that it was more likely to be a portion of the fourth palmar interosseous whose origin had migrated superficially (Mortensen and Pettersen, 1966). This muscle may also be a radial head of flexor digiti minimi which was found in one trisomy 13 hand (Case 4; Dunlap et al., 1986). Wood (1865, 1866, 1867, 1868) and Macalister (1875) give no convincing evidence of the contrahentes in dissection-room cadavers, notwithstanding their knowledge of atavistic musculature (including unusual variations), amongst humans and their wide knowledge of comparative vertebrate anatomy. In his paper on the ontogeny of the hypothenar muscles, Frazer (1908) states that a contrahens V appears briefly in human ontogeny.

The unusual “lumbrical” between digits I and II found in seven trisomy 18 hands may be a displaced slip of contrahens I. Goss (1973, p.484) states that the adductor pollicis “…may receive a slip from the transverse metacarpal ligament.” In Macaca, the adductor pollicis originates, in part, from the second metacarpophalangeal joint capsule (Howell and Straus, 1933). Our observations of catarrhine monkeys and apes concur with this view. However, only in Pongo, was there a separate slip of contrahens originating from the radial side of the proximal phalanx of digit II. This slip was in close proximity to the rest of contrahens I in Pongo. In trisomy 18 hands this slip, i.e. the “lumbrical” between digits I and II, was quite isolated from contrahens I except at the insertion. This isolation initially led us to label it as “lumbrical” (Dunlap et al., 1986). Bryce (1923) states that accessory first lumbrical slips may arise from the tendons of either flexor pollicis longus or flexor digitorum superficialis, metacarpal I, or opponens pollicis. Further, it was usually found in trisomy 18 hands along with anomalous lumbricals and flexor pollicis longus tendons, respectively (see Tables 5 and 7 in Dunlap et al., 1986).

Two studies on the incidence and variations of human lumbricals indicate that the first has the fewest variations (Mehta and Gardner, 1960; Basu and Hazary, 1961). Basu and Hazary (1961) found no unusual variations of the first lumbrical in their sample of 72 hands. Mehta and Gardner (1960) found slight variations in 13 of 75 hands which they dissected. In one of the remaining 62 hands, the first lumbrical originated entirely from the ventral surface of metacarpal III, just distal to the transverse head of adductor pollicis and passed deep to the first dorsal interosseous before inserting on the extensor expansion tendon. Nevertheless, in our trisomy hands the first lumbrical was the most variable, including absence in five trisomy 18 hands (Cases 3 and 8, bilaterally; Case 6, right).

According to Dylevsky (1967, 1968) and Cihak (1972), the lumbricals appear alongside the differentiating tendons of the flexor digitorum profundus, simultaneously with the reabsorption of the ulnarward contrahentes and the formation of contrahens I (adductor pollicis). The latter attains its adult insertion very early in this process but the origin is not yet in place on metacarpal III. It seems likely that the distally-growing flexor digitorum profundus tendons (including flexor pollicis longus tendon at this time) could easily displace loose slips derived from the contrahentes origin and carry them distally and radialward on to digit II.

The ulnarward contrahentes (II, IIII and V have so far only been described in trisomy 18 (Dunlap et al., 1986). This should not be surprising because delayed development in the trisomy 18 hand is also manifested by the following: a high incidence of diminutive superficial thenar musculature (Dunlap et al.,1986), absent thenar musculature (Ramirez-Castro and Bersu, 1978), well-developed deep thenar musculature in the form of opponens pollicis and interosseous palmaris I of Henle, low incidence of the deep head of Cruveilhier, and high incidence of flexor pollicis longus tendon configurations reminiscent of nonhuman primates (Howell and Straus, 1933; Dunlap et al., 1985).

GENERAL DISCUSSION

Based on information regarding human ontogeny, we have argued that several supernumerary intrinsic hand muscles of human aneuploids are homologous with normal musculature of certain adult nonhuman primates. Muscle homologies are established on the basis of similarities in origin, insertion, innervation and development. In the case of the deep head of Cruveilhier, the importance of origin and insertion is open to various interpretations (Day and Napier, 1963). As to relations, the more common radialward insertion and location deep to the tendon of flexor pollicis longus certainly suggest a function more like a short flexor. We contend that innervation, used exclusively, is an equivocal criterion for establishing homologies particularly when attachments are known to migrate during ontogeny or are located between separate nerves (Dunlap et al., 1985). Other investigators have advanced similar arguments based on their studies of other muscles (Haines, 1935; Straus, 1946b; Minkoff, 1974; Jones, 1979). Since thenar muscle attachments are known to migrate during early development (Cihak, 1969, 1972) and the ulnarward margin of these muscles is associated with the border between separate nerve supplies (St, John Brooks, 1886; Day and Napier, 1961; Cihak , 1969; Goss, 1973), we regard innervation, taken exclusively, as a moot criterion for establishing muscle homologies.

Development is probably the most significant criterion for establishing muscle homologies in this instance. The few trisomies that show intermediate stages of thenar muscle development support Cihak’s (1972) demonstration, in normal human embryos, of the development of intrinsic hand muscles. Since extensive embryological studies of muscles are frequently unavailable, the utility of the embryological criterion for homology establishment may be somewhat diminished, especially due to the dearth of similar data in nonhuman primates. However, the ontogenetic retention of ancestral morphological states, however brief, in an otherwise relatively derived human hand, suggests that a consistent early ontogenetic pattern is likely to be found in nonhuman primates.

Invocation of embryological data for analyzing homology has been a long established practice in evolutionary studies (Darwin, 1859). Notwithstanding Haeckel’s simplistic formulation of the Biogenic Law, embryological structures may profitably be used in establishing homologies (Orton, 1955; Waddington, 1957; deBeer, 1958; Simpson, 1961; Mayr, 1969, 1981). Normal human muscle development has been studied for pectoral muscles (Lewis, 1901; Huntington, 1904), extrinsic manual flexors (Dylevsky, 1967, 1968), intrinsic muscles of the hand and foot (Cihak, 1972) and facial muscles (Gasser, 1967). These studies record the transitory appearance of several ancestral muscles not normally occurring in humans beyond the fetal stage.

Human aneuploids invariably manifest delayed development of varying degree (Warkany et al., 1966; Shapiro, 1983). The high incidence of atavistic musculature in the trisomies we have dissected and particularly in intrinsic hand muscles of trisomy 18 (Aziz and Dunlap, 1986; Dunlap et al., 1986) is further evidence of the ubiquitous occurrence of developmental retardation in aneuploidy. According to Shapiro (1975, 1983) increased anatomical variability exhibited by aneuploidy is proportional to that found in chromosomally-normal humans. While this is not precisely the case with all muscles, the variability is clearly not random; there is phenotypic specificity for each human trisomy investigated so far (i.e. trisomies 13, 18 and 21; Opitz et al., 1979; Pettersen and Bersu, 1982; Dunlap et al ., 1986).

Several muscle groups whose ontogeny has been examined in normal humans briefly exhibit the same ancestral pattern which tends to be retained amongst aneuploids. To our knowledge, no aneuploid nonhuman primate has been fully investigated from the myological viewpoint. However the existence of atavistic musculature in such cases would not be surprising. Unfortunately, limb dissections of trisomic Pan troglodytes and Pongo pygmaeus (trisomy 22 cases believed to be homologous to human trisomy 21: McClure, 1972; McClure et al., 1973; Andrle et al., 1979) were not performed. A trisomy ape ( Pongo ?) was recently destroyed at the San Diego Zoo. Theisen et al. (1979) dissected a thalidomide-treated macaque whose forelimb malformations did not resemble any human aneuploid phenotypes. Hill (1962) also reported no muscular variations resembling the latter in a lobster-clawed drill.

In the absence of comprehensive longitudinal studies of human muscle development, the general conditions of delayed development in aneuploid phenotypes renders these natural “genetic experiments” useful as cross checks against serial studies. Thus, thenar muscle variations of the sort found in trisomies are predictable and expected in light of Cihak’s work (1969, 1972). Of particular note are three trisomy 18 hands Case 5, left; Case 9, bilaterally) which had an interosseous palmaris I of Henle and an ulnar head of flexor pollicis brevis. These cases illustrate an intermediate condition for the migration and differentiation of the primitive flexores breves profundi (Haines, 1950, 1955).

The interosseous palmaris I of Henle, as it appears in Cebus, Macaca and the apes, retains more primtive attachments than does the opponens pollicis in any of the primates we studied. Significantly, the former inserts on the proximal phalanx. The occurrence of this muscle in Cebus, was a major factor in arguing for Cebus being a good model for a primitive anthropoid ancestor (Dunlap et al., 1985). The absence of this muscle in other platyrrhines is striking. Although we did not find interosseous palmaris I of Henle in Alouatta palliata, Schon (1968) reported it in Alouatta seniculus. He states that, in the latter, the muscle was inserted on metacarpal I. The only case where we found an “interosseous palmaris I of Henle” inserting on the bone it originated from was in trisomy 13 (Case 4, right). The condition in Alouatta seniculus may be evidence for a consistent early ontogenetic pattern of primate hand musculature discussed above.

The retention of primitive thenar musculature, occasional preaxial skeletal reduction, and the expression of ulnarward contrahentes in trisomy 18 not only exemplify developmental delay, but also appear to manifest an atavistic complex illustrating important evolutionary changes which have occurred amongst hominoids, particularly humans. We have earlier argued that developmental delay in the extensor digitorum profundus complex in human trisomies 13, 18 and 21 manifests similar atavistic phenomena as reported here (Aziz and Dunlap, 1986). These concomitant hand and forearm muscle configurations of developmental delay not only illustrate important evolutionary changes, but may also provide valuable new information about the relationship between ontogeny and phylogeny amongst hominoids.

The genetic bases of the anomalies reported here remains to be satisfactorily explained. Recent findings based on research in molecular cytochemistry and genetics suggest that : 1) the pathogenesis of human aneuploidy is caused by the unbalanced amount of nonstructural, or repetitive DNA, and , 2) the atavistic structures which appear in aneuploids simultaneously provide evidence of how those structures evolved and how normal development proceeds. No genetic material that codes for a protein, enzyme or other biochemical product has been shown to play a clear role in aneuploid pathogenesis (Schweber, 1985; Cooper and Hall, 1988). In their review of trisomy 21 Cooper and Hall (1988, p.507) state that “… little is known of the mechanisms by which the extra chromosome exerts its pathologic effects.” These authors emphasize that genes causing trisomy 21 have not been identified and that a complete knowledge of chromosome 21, particularly the pathological segment 21q22, is essential for understanding the pathology. Other recent work suggests a similar view (Schweber, 1985; Vogel and Mutolsky, 1986; Shapiro, 1989; Stewart et al., 1989; Speicher et al., 2010). In their discussion of repetitive DNA on chromosome 21 Cooper and Hall (1988) cite evidence for members of the Alu sequences on chromosome 21, also located on chromosomes 13, 18 and 22.

The ubiquitous nature of developmental instability in aneuploids stands in marked contrast to the rarity of biochemical abnormalities associated with point mutations in these same gross chromosomal abnormalities (Rhode, 1965; Vogel, 1973; Smith, 1977). The postnatal retention of abnormal amounts of fetal hemoglobin in trisomy 13 (Yunis and Hook, 1966) is a manifestation of developmental delay and should not be confused with specific point mutations. The structural genetic material for hemoglobin is located on chromosomes 11 and 16. Lewandowski and Yunis (1977) suggested that regulatory genetic material may be located on chromosome 13. Schweber (1985), Cooper and Hall (1988) and Shapiro (1989) have proposed that regulatory proteins active during development may play an important role in aneuploid pathophysiology.

We believe that the developmental instability and retardation seen in all aneuploid anatomical and physiological systems may be due to the abnormal amount of nonstructural DNA. Moreover, we hypothesize that the association of developmental retardation, atavistic musculature, and the absence in aneuploids of biochemical abnormalities resulting from specific point mutations support the proposition that evolution may primarily involve nonstructural DNA, Many investigators (deBeer, 1958; Waddington,1975; King and Wilson, 1975; Jacob, 1977; Alberch, 1980; Raff , 1990; Fondon and Garner,2004) suggest that changes in the timing of development rather than advantageous mutations in structural DNA may frequently be responsible for evolutionary change. Shea (1987) has explored at length the importance of heterochrony in hominid evolution (see also Hall, 1984; Wilson, 1988).

In primates there is a close similarity between enzymes, proteins and other biochemical products which contrasts markedly with the gross phenotypic differences (Yunis and Yasmineh, 1971; King and Wilson, 1975; Dutrillaux, 1979). The chromosomes of primates have been extensively investigated in 60 species by Dutrillaux, (1979; p. 280), who comments “…that it appears quite probable that all species of Primates we analyzed possess the same euchromatic segments (the same nonvariable R and Q bands). The only quantitative variations we observed concerned exclusively the heterochromatin.” Heterochromatin contains much of the repetitive DNA (Yunis and Yasmineh, 1971) which has been hypothesized to, at least partially, be responsible for controlling ontogeny and the expression of structural DNA (Davidson and Britten, 1973, 1979; Guille and Quetier, 1973; Holliday and Pugh, 1975; Davidson et al., 1983). Of course, many structural genes are surrounded by repetitive DNA (Vogel and Mutolsky, 1986; Vogt, 1990). This may be particularly important since the pathological segments of the common human trisomies, 13, 18 and 21, appear to contain large portions of euchromatin (Turleau et al., 1980; Cooper and Hall, 1988; Vogt, 1990; Speicher et al., 2010).

Vogel (1973) is amongst the earliest to suggest that aneuploid phenotypes in humans are related to disturbances in nonstructural DNA of a regulatory nature. There is evidence that repetitive DNA is transcribed and possibly plays a role in the regulation of development and in oncogenetic transformations (Davidson and Posakony, 1982; Murphy et al., 1983; Wharton et al., 1985). Wharton et al. (1985) and Bodnar and Ward (1987) present evidence and discuss the possibility of short repetitive DNA elements in eukaryotes being involved in development and gene expression. Bodnar and Ward (1987) show that short repetitive elements are homologous to known regulatory sequences and oncogenes. Repetitive DNA appears to be involved with the timing or regulatory mechanisms in the period mutants of circadian rhythm genes in Drosophila (Leclerc and Regier, 1990). Nordstrom (1990) has shown that repetitive DNA appears to be employed in bacterial plasmids and even some eukaryotic plasmids for controlling replication frequency. Desplan et al., (1988) present evidence that repeat units in the Drosophila homeodomain may affect the timing or concentration of gene expression by their location and/or number of repeats. Holliday and Pugh (1975) hypothesized that demethylation might provide a mechanism for initiating gene expression in some instances, Erlich and Wang (1981) and Doerfler (1983) have shown that demethylation is involved in some cases of gene expression in eukaryotes. More recent work continues to support this relationship and to link demethylation with repetitive DNA sites (Magill and Magill, 1989; Cedar, 1988; Paroush et al., 1990; Bodnar and Ward, 1987). Ever mindful of the many developmental mechanisms which must operate between genotype and phenotype, we find Alice’s experience at the Mad Tea Party (Carroll, 1990) analogous to our incomplete knowledge. Many of Alice’s difficulties were with time and although there was no misunderstanding that the table was “...laid for a great many more than three.” (p. 83) just how many more and how frequent the moves occurred was never clear (see Fig. 3, after Tenneil). Development and tea are highly regular and repeated events.

 

Unraveling the final details of developmental processes at all levels is underway.

figure 3

Figure 3 After John Tenneil
“Then you keep moving round, I suppose?” said Alice.
“Exactly so.” said the Hatter: “as the things get used up.”

 

Many developmental mechanisms must operate between genotype and phenotype. The advance in our knowledge of the relationship between genotype and phenotype is well-illustrated by the discovery of highly conserved homeo-box sequences in Drosophila, Xenopus. Mus, Homo and other species (Joyner et al., !985; Rabin et al., 1985). The homeo-box sequences in Drosophila are associated with developmental events (Nusslein-Volhard and Wieschaus, 1980; McGinnis et al., 1984). The vast evolutionary distance separating these species which share homologous sequences suggest similar functions for the sequences. Rabin et al., (1985) also indicate that the sequences in Mus and Homo are located in homologous chromosomal regions. A study of D. melanogaster heterochromatin (Smith et al., 2007) demonstrated significant conservation of protein coding genes across other fly, insect and even vertebrate species. The high content of repetitive elements with the exons in these heterochromatic regions suggests their study in flies will improve study and understanding of the comparable heterochromatin in humans. In another study the Hox genes in squamate evolution (Di-Poi et al., 2010) were found to differ significantly in those areas of antero-posterior axis boundaries associated with snake and lizard vertebral and rib evolution, Additionally (presumably coincidentally) , findings demonstrated “... strong variations in both the presence and the length of monotonic amino acid repeats...” A paper by Fondon and Garner (2004) strongly suggests that morphological evolution may be closely associated with repetitive DNA. Repetitive element variations were found to be related to significant morphological variations in developmental genes for the forelimb and the skull in domestic dogs. Although these investigations involved artificial selection in Canines, and, not withstanding the importance of cis regulatory sequences in development and evolution (Davidson, 2010; Speicher et al., 2010) , research on repetitive DNA will eventually prove to be crucial in our understanding of morphological variation and evolution in eukaryotes and many developmental malformation syndromes including trisomies. Not surprisingly, “junk DNA” appears after all not to be junk (Keller, 2011).

 

Table 1

legend table 1

 

Table 2

 

ACKNOWLEDGMENTS

We are grateful to the parents who donated deceased human trisomy fetuses and neonates for this investigation and to the following clinicians who facilitated donations: Drs. D. S. Borgaonkar, J.C. Carey, S. Dempsey, J.C. Pettersen, K.N. Rosenbaum, T.H. Shepard, R.B. Surana, B.A. Quinton and K. Toomey. R. M, Tyler and J. Ferguson assisted in embalming and preparing many of the human specimens. We thank Dr. Richard W. Thorington, Jr,, for valuable discussions , dissections and in loaning many of the nonhuman primates. We also are grateful to Dr. Harold M. McClure for assistance in obtaining ape specimens. We thank Ms Marie T. Dauenheimer for the illustrations. Finally, we are grateful for dissection assistance by Anna LeValley and Emilyann Pafford. This work was supported in part by NIH Grant # 5 R01 HD13644 to Dr. Aziz.

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