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Bipartition of the superior articular facets of the first cervical vertebra (atlas or C1): a human variant probably specific among primates
ARTICLE IN PRESS Ann Anat 189 (2007) 79—85
www.elsevier.de/aanat
Bipartition of the superior articular facets of the first cervical vertebra (atlas or C1): a human variant probably specific among primates Franck Billmanna, Jean-Marie Le Minora,, Matthias Steinwachsb a
Institute of Normal Anatomy (EA 3428), Faculty of Medicine (ULP), F-67085 Strasbourg, France Department of Orthopaedic Surgery, Albert Ludwig University of Freiburg, Hugstetter Str. 55, D-79106 Freiburg, Germany
b
Received 17 May 2006; accepted 11 July 2006
KEYWORDS Cervical spine; Cranio-vertebral junction; Joint variants; Physical anthropology; Primates
Summary The bipartition of the superior articular facet is one of the classical variants of the human atlas. Rare quantitative data are available in the literature on this possible bipartition in humans and this disposition remains little understood. For non-human primates, there are almost no detailed comparative data in the literature, despite their potential importance in understanding the significance of this pattern in humans and its evolution. The material used in this study consisted of 500 human atlases and of 256 atlases of non-human primates representing 37 genera. In humans, bipartition of one or both of the superior articular facets was observed in 104 individuals out of the 500 (20.8%); bilateral occurrence was observed in 46.2% of the bipartitions and unilateral occurrence in 53.8%; no significant right or left predominance was observed. In non-human primates, no case of bipartition of the superior articular facets of the atlas was found in any of the 256 individuals studied. From a phylogenetic point of view, we suggest that a single superior facet of the atlas is the primitive pattern or plesiomorphy in primates. Modification of this general pattern seems to occur only in some individuals in Homo sapiens within primates, and the bipartition of the facet could thus be interpreted as a derived characteristic restricted to the human species or autapomorphy. The appearance of the bipartition of the superior articular facet of the atlas during human evolution could be the result of functional modifications due to the acquisition of constant erect posture and bipedalism. & 2006 Elsevier GmbH. All rights reserved.
Corresponding author. Tel.: ++3 88 365365; fax: ++3 88 365365.
E-mail address: [email protected] (J.-M. Le Minor). 0940-9602/$ - see front matter & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.aanat.2006.07.007
ARTICLE IN PRESS 80
F. Billmann et al.
Introduction
Materials and methods
Anatomical variants of the first cervical vertebra or atlas in humans have already been noted in early works (Allen, 1879; Macalister, 1893; Le Double, 1912; Dubreuil-Chambardel, 1921; Bergman, 1967). The significance of most of these variants remains poorly understood and the explanations proposed are essentially theoretical. Comparative anatomy often sheds new light on the significance of anatomical variations and on the evolution of morphological structures. The use of a comparative approach has thus allowed the demonstration: (1) that the retrotransverse foramen is a derived trait only observed in some human individuals (autapomorphy) within primates (Le Minor, 1997), and (2) that the presence of the lateral ponticle and/or the dorsal ponticle over the groove for the vertebral artery observed in some human individuals can be interpreted as the persistence of primitive characteristics (plesiomorphy) throughout the progressive disappearance of these ponticles and is an evolutionary tendency characteristic of primates and particularly of hominoid evolution (Le Minor and Trost, 2004). The bipartition of the superior articular facet of the atlas is one of the classical variants of the human atlas (no. 27 in the list of infracranial nonmetric variants of Finnegan (1978)). The left and right superior articular facets (foveae articulares craniales atlantis), supported by the lateral masses and articulated with the respective occipital condyles, are single and reniform with their long axes converging anteriorly (Williams, 1995); however, great variability in the shape of outlines has been described from oval elongated to reniform or kidney-shaped, with the presence of various constrictions, and with frequent asymmetrical aspects (Singh, 1965; Tillmann and To ¨ndury, 1987). Rare quantitative data are available in the literature on this possible bipartition in humans and this disposition remains little understood. For non-human primates, there are almost no detailed and precise comparative data in the literature, despite their potential importance in understanding the significance of this pattern in humans and its evolution. The aim of the present study, based on extensive human and comparative vertebral samples, was to provide original observations in order to attempt to understand the bipartition of the superior articular facet of the human atlas, to ascertain its occurrence in primates, and to offer some elements regarding the evolutionary and functional significance of this disposition.
The material used in this study consisted of 500 human atlases (Homo sapiens) and of 256 atlases of non-human primates representing 37 genera. These vertebrae (dried bones) came from adult subjects without pathological signs in the cervical spine. The precise age and sex were unknown. The 256 atlases of non-human primates were distributed as follows: Prosimii (61 individuals from 13 genera): Lemuridae: 2 Hapalemur, 23 Eulemur; Indriidae: 1 Avahi, 3 Indri, 7 Propithecus; Daubentoniidae: 2 Daubentonia; Cheirogaleidae: 3 Cheirogaleus, 6 Microcebus; Galagidae: 3 Galago; Lorisidae: 2 Loris, 3 Nycticebus, 3 Perodicticus; Tarsiidae: 3 Tarsius; Platyrrhinii (35 individuals from 11 genera): Callitrichidae: 6 Callithrix, 1 Leontopithecus, 1 Saguinus; Cebidae: 2 Aotus, 9 Cebus, 3 Saimiri; Atelidae: 1 Alouatta, 6 Ateles, 1 Cacajao, 3 Lagothrix, 2 Pithecia; Catarrhinii (99 individuals from 9 genera): Cercopithecinae: 7 Cercocebus, 21 Cercopithecus, 3 Erythrocebus, 27 Macaca, 28 Papio, 4 Theropithecus; Colobinae: 2 Colobus, 2 Nasalis, 5 Presbytis; Hominoidea (61 individuals from 4 genera): 13 Hylobates, 16 Gorilla gorilla, 19 Pan troglodytes, 13 Pongo pygmaeus. These vertebrae belong to the following collections: (1) Laboratoire d’Anatomie and Muse´e Delmas-Orfila-Rouvie `re (UFR des Saints-Pe `res, Paris, France), (2) Laboratoire d’Anatomie Compare ´e (Muse´um National d’Histoire Naturelle, Paris, France), (3) Laboratoire d’Anatomie (Faculte´ de Me´decine, Tours, France), (4) Institut d’Anatomie Normale (Faculte´ de Me´decine, Strasbourg, France), (5) Muse´e Zoologique (Strasbourg, France), (6) Laboratoire d’Anatomie (Faculte´ de Me´decine, Nancy, France), (7) Ecole du Service de Sante´ des Arme ´es (Lyon, France), (8) Institut fu ¨r Anatomie (Wien, Oesterreich). For each atlas, we studied the morphology of the left and right superior articular facets focusing on a possible bipartition. The bipartition was noted as present only if it was complete with two welldefined facets separated by a clear non-articular groove or area; the partial forms were not recorded. This bipartition was sometimes present on both sides, present only on the right side, present only on the left side, or absent.
Results In humans, bipartition of one or both of the superior articular facets of the atlas was observed in 104 individuals out of the 500 in the present
ARTICLE IN PRESS Bipartition of superior facets of the atlas
81
series (20.8%) (detailed results in Table 1). Bilateral occurrence (symmetric manifestation) was observed in 46.2% of the bipartitions and unilateral occurrence in 53.8%. No significant right or left predominance was observed in the frequency of lateral occurrence even if bipartitions were slightly more numerous on the right side (detailed results in Table 2). When a bipartition existed, the morphology of each of the two facets was variable: circular or elliptical; however, in most cases the ventral facet was more or less elliptical and the dorsal facet quite circular. The sizes of the facets were also variable: in some cases the ventral and dorsal facets presented similar sizes, in some cases the
Figure 2. Bilateral bipartition of the superior articular facets of the human atlas, with an elliptical anterior facet and a circular posterior one (superior view).
Table 1. Individual occurrence of bipartition of the superior articular facets in the 500 human atlases of the present series Bipartition
Bilateral Unilateral Left Unilateral Right Total
Number of cases
Frequency (%)
Relative frequency (%)
48 23 33
9.6 4.6 6.6
46.2 22.1 31.7
104
20.8
100.0
Table 2. Side occurrence of bipartition of the superior articular facets in the 500 human atlases of the present series Bipartition Left side Right side Total
Number of cases
Figure 3. Right unilateral bipartition of the superior articular facets of the human atlas, with an elliptical anterior facet and a circular posterior one (superior view).
Frequency (%)
71 81
14.2% 16.2%
152
15.2%
ventral facet was slightly smaller and in others slightly greater. The non-articular area or groove separating the two facets in bipartite cases was situated quite transversally around the middle part of the entire articular area and corresponded to the strangled part of the classical unique facet. The non-articular area was rough and at a deeper level than the articular facets (Figs. 1–3). In non-human primates, no case of bipartition of the superior articular facets of the atlas was found in any of the 256 individuals studied.
Discussion Figure 1. Superior articular facets of the human atlas. Classical reniform or kidney-shaped aspect of both left and right facets with a constriction or strangled part at their mid-length (superior view).
Occurrence of bipartition in humans Precise data concerning the frequency of the bipartition of the superior articular facets of the
ARTICLE IN PRESS 82 Table 3.
F. Billmann et al. Frequency of bipartition of the superior articular facets of the atlas in the main series of the literature
Authors
Number of cases
Number of bipartition
Frequency of bipartition (%)
Dubreuil-Chambardel (1921) Gottlieb (1994) Hasebe (1913) Le Double (1912) Macalister (1893) Poirier (1896) Prescher (1997) Singh (1965) Tsusaki (1924) Present series
Approx. 500 30 100 500 – 500 200 200 22 500
– 7 0 – – – 28 19 2 104
16.0 23.3 0.0 6.1 5.7 Approx. 10.0 14.0 9.5 9.1 20.8
Dash (–): number not precised in the original study.
Table 4. Individual occurrence of bipartition of the superior articular facets of the atlas in the main series of the literature
Table 5. Side occurrence of bipartition of the superior articular facets of the atlas in the main series of the literature
Authors
Authors
Left
Right
5 (16.7%) 13 (6.5%) 13 (6.5%) 71 (14.2%)
4 (13.3%) 24 (12.0%) 9 (4.5%) 81 (16.2%)
Gottlieb (1994) Le Double (1912) Macalister (1893) Prescher (1997) Singh (1965) Present series
Bilateral
2 (28.6%) – (57.4%) – (52.6%) 9 (32.1%) 3 (15.8%) 48 (46.2%)
Unilateral Left
Right
Gottlieb (1994)
3 (42.8%) – – – – 4 (14.3%) 10 (52.6%) 23 (22.1%)
2 (28.6%) – – – – 15 (53.6%) 6 (31.6%) 33 (31.7%)
Prescher (1997)
Dash (–): number not precised in the original study.
human atlas are scarce; the data of the main series of the literature are given in Tables 3–5. There are no data available which specify variations of this bipartition according to sex or age; however, on the whole, the results obtained on the existence of differences in the incidence of expression of other non-metrical traits between males and females, or at various ages, are either negative or show little consistency (Hauser and De Stefano, 1989). Geographical origin could be a factor of intraspecific variation of the frequency of bipartition within human populations even if most series available are based on European individuals. The frequency of bipartition seems to be similar in Indian (Singh, 1965), Formosan (Tsusaki, 1924), and European populations (Table 3). Bipartition seems to be rarer or even absent in Japanese populations as suggested by the absence of any case of bipartition in the 100 individuals studied by Hasebe
Singh (1965) Present series
(1913). For other non-metric variants of the human atlas, and in particular for the bony ponticles over the groove for the vertebral artery, particularities in the frequencies also seem to exist in Japanese populations (review in Le Minor and Trost, 2004). Characterization of a trait as simply present or absent ignores a wider range of variation, which corresponds to the biological reality of variable degrees of expression of traits (Hauser and De Stefano, 1989). However, the difficulty in defining transition types is a source of confusion, and the resulting lack of reproducibility between observers leads to difficulty in comparing data sets (Finnegan, 1978). This is why we decided to consideronly the complete bipartition of the superior articular facets of the atlas as being present; further attempts should be made to determine how to reliably quantify partial forms. When scoring bilateral non-metrical traits three different modes of approach exist (Trinkaus, 1978; Green et al., 1979; Korey, 1980; Hauser and De Stefano, 1989). In the first approach, each of the two sides are scored separately, taking into account bilateral as well as unilateral occurrence; this allows for the determination of side incidence as
ARTICLE IN PRESS Bipartition of superior facets of the atlas well as individual incidence, and for identification of asymmetry of expression. In the second approach, the two sides are scored separately, without taking into consideration the trait on the other side; this allows for the determination of side incidence only. In the third approach, the traits are scored by individuals, only indicating whether the individual shows the trait or not; this allows for the determination of individual incidence only. The choice of sampling by individuals or by sides is most frequently dictated by the exigencies imposed by the fragmentation of the material. We used the first approach, which gives the fullest information; it is, however, easier for an axial structure such as the atlas vertebra in which left and right structures are located on the same bone. The frequency of bilateral occurrence of a trait is generally higher than the frequency expected if combinations of left- and right-sided expressions occurred only at random (independence of the two sides) (Trinkaus, 1978; Green et al., 1979; Korey, 1980; Hauser and De Stefano, 1989). In the case of the bipartition of the superior articular facets of the atlas, very few data are available in the literature concerning its symmetry; the frequency of bilateral occurrence varies between 15.8% and 57.4% according to the series (main results in Table 4). The expression of the bipartition on the left and right sides appear thus to be linked; however, in total, the frequency of asymmetrical occurrences is similar to symmetrical ones or even predominant. Laterality is the tendency of a unilaterally expressed trait to occur more frequently on one side than on the other. In most non-metric cranial traits, there is no convincing evidence of consistent laterality (Hauser and De Stefano, 1989). In the case of the bipartition of the superior articular facets of the atlas, the present study demonstrates similarly that no substantial difference exists between left (14.2%) and right (16.2%) occurrences (Table 2); the rare data in the literature are controversial (Table 5). A tendency to have larger facets on the right side than on the left side has been observed by Mysorekar and Nandedkar (1986) who measured their area in 103 atlases.
Occurrence of bipartition in non-human primates The observations of the present study suggest that the bipartition of the superior articular facet of the atlas does not exist in non-human primates. This also seems to be supported by the data of the literature which are, however, very poor and vague on this trait (Schultz, 1955, 1961; Hartman and
83 Straus, 1933; Olivier and Laffont, 1964; Ankel, 1967; Lessertisseur and Saban, 1967). The main difference between apes and modern humans seems only to consist in superior atlantal facets which are more concave in apes (Aiello and Dean, 1990).
Evolutionary and functional significance From a phylogenetic point of view, a single superior facet of the atlas seems to be the primitive pattern or plesiomorphy in primates as suggested by the comparative data. Modification of this general pattern seems to occur only in some individuals in H. sapiens within primates, and the bipartition of the facet could thus be interpreted as a derived characteristic restricted to the human species or autapomorphy. It is tempting to interpret the appearance of the bipartition of the superior articular facet of the atlas during human evolution as the result of functional modifications due to the acquisition of constant erect posture and bipedalism. The relationships between the evolution of hominoid posture and the positions of the foramen magnum and the occipital condyles have been widely studied (Schultz, 1955; Dean and Wood, 1981, 1984; Aiello and Dean, 1990; Luboga and Wood, 1990; Ahern, 2005). An antero-inferiorly positioned and vertically orientated foramen magnum has been considered linked to erect posture and bipedalism and thus specific to fossil and modern H. sapiens. This forward placement of the foramen magnum in humans has been interpreted as an essential adaptation to balance the head more efficiently on a vertical and erect spine; it has clearly had an effect upon the forces required to move and balance the head and there have been accompanying changes to the cervical muscles. In this context, the constraints in the human atlanto–occipital joint have obviously been modified and the bipartition observed in some individuals could be the reflection of these modifications. A similar bipartition has been described for the human occipital condyles; further studies would be necessary to ascertain whether the bipartitions of the occipital and atlantal facets are always linked (Berry and Berry, 1967; Hauser and De Stefano, 1989). Greater pressures on the anterior and posterior portions of the facet have been proposed by some authors as being the functional factors at the origin of the bipartition (Singh, 1965; Tillmann and Lorenz, 1978). Two roughly circular pressure facets are indeed present and evident in many individuals
ARTICLE IN PRESS 84 in the anterior and posterior parts of the superior articular facets of the atlas even in atlases which show no signs of division; in some cases these are so marked that the rest of the articular area looks non-articular (Singh, 1965). Tillmann and Lorenz (1978) suggested that the bipartition of the corresponding occipital facets in human adults is not controlled genetically, but has an individual mechanical causality and is due to stresses in the postnatal years. Considering the regular shape of the bipartite facets and the regular aspect of the subchondral bone, we suggest, on the contrary, that the bipartition is under genetic control and is the result of a phylogenetic process during which only the articular area submitted to mechanical stresses remains, the area less subjected to mechanical strain tending gradually to become non-articular. The significance of unilateral occurrences or asymmetric manifestations (42.6–84.2% according to the series; Table 4) versus bilateral occurrence or symmetric manifestation could simply be the reflection of a general rule for rare or inconstant traits for which a predictable relationship exists between the frequency of non-metric traits and the probability that they are expressed bilaterally as already demonstrated for cranial non-metric traits (Hallgrimsson et al., 2005). Thus, unilateral occurrences are probably not purely the reflection of asymmetric mechanical constraints. Such unilateral occurrences are similarly observed for all other non-metric traits of the human atlas such as ponticles (Le Minor, 1997; Van Roy et al., 1997; Le Minor and Trost, 2004). The frequent asymmetry in the disposition of the superior articular facet of the atlas probably implies functionally that true symmetry of segmental movement may not be possible in corresponding individuals and is not pathological but only a normal variant; this is of interest for the design of certain chiropractic theories and/or techniques which rely on symmetry as being normal (Van Roy et al., 1997).
Acknowledgment We particularly thank Miss Kate Welch for her help in checking the English language.
References Ahern, J.C., 2005. Foramen magnum position variation in Pan troglodytes, Plio–Pleistocene hominids, and recent Homo sapiens: implications for recognizing the
F. Billmann et al. earliest hominids. Am. J. Phys. Anthropol. 127, 267–276. Aiello, L., Dean, C., 1990. An Introduction to Human Evolutionary Anatomy. Academic Press, London. Allen, W., 1879. On the varieties of the atlas in the human subject, and the homologies of its transverse processes. J. Anat. 14, 18–28. Ankel, F., 1967. Morphologie von Wirbelsa ¨ule und Brustkorb. Primatologia 4, 1–120. Bergman, P., 1967. On varieties of the atlas in man. Folia Morphol. 26, 129–139. Berry, A.C., Berry, R.J., 1967. Epigenetic variation in the human cranium. J. Anat. 101, 361–379. Dean, M.C., Wood, B.A., 1981. Metrical analysis of the basicranium of extant hominoids and Australopithecus. Am. J. Phys. Anthropol. 59, 53–71. Dean, M.C., Wood, B.A., 1984. Phylogeny, neoteny and growth of the cranial base in hominoids. Folia Primatol. 43, 157–180. Dubreuil-Chambardel, L., 1921. L’atlas. Vigot, Paris. Finnegan, M., 1978. Non-metric variation of the infracranial skeleton. J. Anat. 125, 23–37. Gottlieb, M.S., 1994. Absence of symmetry in superior articular facets on the first cervical vertebra in humans: implications for diagnosis and treatment. J. Manip. Physiol. Ther. 17, 314–320. Green, R.F., Suchey, J.M., Gokhale, D.V., 1979. The statistical treatment of correlated bilateral traits in the analysis of cranial material. Am. J. Phys. Anthropol. 50, 629–634. Hallgrimsson, B., Donnabhain, B.O., Blom, D.E., Lozada, M.C., Willmore, K.T., 2005. Why are rare traits unilaterally expressed?: trait frequency and unilateral expression for cranial nonmetric traits in humans. Am. J. Phys. Anthropol. 128, 14–25. Hartman, C.G., Straus, W.L., 1933. The anatomy of the Rhesus monkey (Macaca mulatta). Hafner, New York. Hasebe, K., 1913. Die Wirbelsau ¨le der Japaner. Z. Morphol. Anthropol. 15, 259–380. Hauser, G., De Stefano, G.F., 1989. Epigenetic Variants of the Human Skull. Schweizerbart, Stuttgart. Korey, K.A., 1980. The incidence of bilateral nonmetric skeletal traits: a reanalysis of sampling procedures. Am. J. Phys. Anthropol. 53, 19–23. Le Double, A.F., 1912. Traite´ des variations de la colonne verte´brale de l’homme. Vigot, Paris. Le Minor, J.M., 1997. The retrotransverse foramen of the human atlas vertebra. A distinctive variant within primates. Acta Anat. 160, 208–212. Le Minor, J.M., Trost, O., 2004. Bony ponticles of the atlas (C1) over the groove for the vertebral artery in humans and primates: polymorphism and evolutionary trends. Am. J. Phys. Anthropol. 125, 16–29. Lessertisseur, J., Saban, R., 1967. Squelette appendiculaire. In: Grasse´, P.P. (Ed.), Traite´ de zoologie. T. 16, Fasc. 1. Masson, Paris, pp. 584–708. Luboga, S.A., Wood, B.A., 1990. Position and orientation of the foramen magnum in higher primates. Am. J. Phys. Anthropol. 81, 67–76.
ARTICLE IN PRESS Bipartition of superior facets of the atlas Macalister, A., 1893. Notes on the development and variations of the atlas. J. Anat. 27, 519–542. Mysorekar, V.R., Nandedkar, A.N., 1986. Surface area of the atlanto–occipital articulations. Acta Anat. 126, 223–225. Olivier, G., Laffont, J., 1964. Les verte `bres du Semnopithe `que. Mammalia 28, 474–518. Poirier, P., 1896. Traite´ d’anatomie humaine, second ed. t. 1. Masson, Paris. Prescher, A., 1997. The craniocervical junction in man, the osseous variations, their significance and differential diagnosis. Anat. Anz. 179, 1–19. Schultz, A.H., 1955. The position of the occipital condyles and of the face relative to the skull base in primates. Am. J. Phys. Anthropol. 13, 97–120. Schultz, A.H., 1961. Vertebral column and thorax. Primatologia 4, 1–66. Singh, S., 1965. Variations of the superior articular facets of atlas vertebrae. J. Anat. 99, 565–571.
85 Tillmann, B., Lorenz, R., 1978. The stress at the human atlanto–occipital joint I. The development of the occipital condyle. Anat. Embryol. 153, 269–277. Tillmann, B., To ¨ndury, G., 1987. Rauber/Kopsch Anatomie des Menschen. I. Bewegungsapparat. Georg Thieme, Stuttgart, New York. Trinkaus, E., 1978. Bilateral asymmetry of human skeletal non-metric traits. Am. J. Phys. Anthropol. 49, 315–318. ¨ ber den Atlas und Epistropheus bei Tsusaki, T., 1924. U den eingeborenen Formosanern (Seiban). Folia Anat. Japan 2, 221–246. Van Roy, P., Caboor, D., De Boelpaep, S., Barbaix, E., Clarys, J.P., 1997. Left–right asymmetries and other common anatomical variants of the first cervical vertebra. Manual Ther. 2, 24–36. Williams, P.L. (Ed), 1995. Gray’s Anatomy, 38th ed. Churchill Livingstone, New York.
www.elsevier.de/aanat
Bipartition of the superior articular facets of the first cervical vertebra (atlas or C1): a human variant probably specific among primates Franck Billmanna, Jean-Marie Le Minora,, Matthias Steinwachsb a
Institute of Normal Anatomy (EA 3428), Faculty of Medicine (ULP), F-67085 Strasbourg, France Department of Orthopaedic Surgery, Albert Ludwig University of Freiburg, Hugstetter Str. 55, D-79106 Freiburg, Germany
b
Received 17 May 2006; accepted 11 July 2006
KEYWORDS Cervical spine; Cranio-vertebral junction; Joint variants; Physical anthropology; Primates
Summary The bipartition of the superior articular facet is one of the classical variants of the human atlas. Rare quantitative data are available in the literature on this possible bipartition in humans and this disposition remains little understood. For non-human primates, there are almost no detailed comparative data in the literature, despite their potential importance in understanding the significance of this pattern in humans and its evolution. The material used in this study consisted of 500 human atlases and of 256 atlases of non-human primates representing 37 genera. In humans, bipartition of one or both of the superior articular facets was observed in 104 individuals out of the 500 (20.8%); bilateral occurrence was observed in 46.2% of the bipartitions and unilateral occurrence in 53.8%; no significant right or left predominance was observed. In non-human primates, no case of bipartition of the superior articular facets of the atlas was found in any of the 256 individuals studied. From a phylogenetic point of view, we suggest that a single superior facet of the atlas is the primitive pattern or plesiomorphy in primates. Modification of this general pattern seems to occur only in some individuals in Homo sapiens within primates, and the bipartition of the facet could thus be interpreted as a derived characteristic restricted to the human species or autapomorphy. The appearance of the bipartition of the superior articular facet of the atlas during human evolution could be the result of functional modifications due to the acquisition of constant erect posture and bipedalism. & 2006 Elsevier GmbH. All rights reserved.
Corresponding author. Tel.: ++3 88 365365; fax: ++3 88 365365.
E-mail address: [email protected] (J.-M. Le Minor). 0940-9602/$ - see front matter & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.aanat.2006.07.007
ARTICLE IN PRESS 80
F. Billmann et al.
Introduction
Materials and methods
Anatomical variants of the first cervical vertebra or atlas in humans have already been noted in early works (Allen, 1879; Macalister, 1893; Le Double, 1912; Dubreuil-Chambardel, 1921; Bergman, 1967). The significance of most of these variants remains poorly understood and the explanations proposed are essentially theoretical. Comparative anatomy often sheds new light on the significance of anatomical variations and on the evolution of morphological structures. The use of a comparative approach has thus allowed the demonstration: (1) that the retrotransverse foramen is a derived trait only observed in some human individuals (autapomorphy) within primates (Le Minor, 1997), and (2) that the presence of the lateral ponticle and/or the dorsal ponticle over the groove for the vertebral artery observed in some human individuals can be interpreted as the persistence of primitive characteristics (plesiomorphy) throughout the progressive disappearance of these ponticles and is an evolutionary tendency characteristic of primates and particularly of hominoid evolution (Le Minor and Trost, 2004). The bipartition of the superior articular facet of the atlas is one of the classical variants of the human atlas (no. 27 in the list of infracranial nonmetric variants of Finnegan (1978)). The left and right superior articular facets (foveae articulares craniales atlantis), supported by the lateral masses and articulated with the respective occipital condyles, are single and reniform with their long axes converging anteriorly (Williams, 1995); however, great variability in the shape of outlines has been described from oval elongated to reniform or kidney-shaped, with the presence of various constrictions, and with frequent asymmetrical aspects (Singh, 1965; Tillmann and To ¨ndury, 1987). Rare quantitative data are available in the literature on this possible bipartition in humans and this disposition remains little understood. For non-human primates, there are almost no detailed and precise comparative data in the literature, despite their potential importance in understanding the significance of this pattern in humans and its evolution. The aim of the present study, based on extensive human and comparative vertebral samples, was to provide original observations in order to attempt to understand the bipartition of the superior articular facet of the human atlas, to ascertain its occurrence in primates, and to offer some elements regarding the evolutionary and functional significance of this disposition.
The material used in this study consisted of 500 human atlases (Homo sapiens) and of 256 atlases of non-human primates representing 37 genera. These vertebrae (dried bones) came from adult subjects without pathological signs in the cervical spine. The precise age and sex were unknown. The 256 atlases of non-human primates were distributed as follows: Prosimii (61 individuals from 13 genera): Lemuridae: 2 Hapalemur, 23 Eulemur; Indriidae: 1 Avahi, 3 Indri, 7 Propithecus; Daubentoniidae: 2 Daubentonia; Cheirogaleidae: 3 Cheirogaleus, 6 Microcebus; Galagidae: 3 Galago; Lorisidae: 2 Loris, 3 Nycticebus, 3 Perodicticus; Tarsiidae: 3 Tarsius; Platyrrhinii (35 individuals from 11 genera): Callitrichidae: 6 Callithrix, 1 Leontopithecus, 1 Saguinus; Cebidae: 2 Aotus, 9 Cebus, 3 Saimiri; Atelidae: 1 Alouatta, 6 Ateles, 1 Cacajao, 3 Lagothrix, 2 Pithecia; Catarrhinii (99 individuals from 9 genera): Cercopithecinae: 7 Cercocebus, 21 Cercopithecus, 3 Erythrocebus, 27 Macaca, 28 Papio, 4 Theropithecus; Colobinae: 2 Colobus, 2 Nasalis, 5 Presbytis; Hominoidea (61 individuals from 4 genera): 13 Hylobates, 16 Gorilla gorilla, 19 Pan troglodytes, 13 Pongo pygmaeus. These vertebrae belong to the following collections: (1) Laboratoire d’Anatomie and Muse´e Delmas-Orfila-Rouvie `re (UFR des Saints-Pe `res, Paris, France), (2) Laboratoire d’Anatomie Compare ´e (Muse´um National d’Histoire Naturelle, Paris, France), (3) Laboratoire d’Anatomie (Faculte´ de Me´decine, Tours, France), (4) Institut d’Anatomie Normale (Faculte´ de Me´decine, Strasbourg, France), (5) Muse´e Zoologique (Strasbourg, France), (6) Laboratoire d’Anatomie (Faculte´ de Me´decine, Nancy, France), (7) Ecole du Service de Sante´ des Arme ´es (Lyon, France), (8) Institut fu ¨r Anatomie (Wien, Oesterreich). For each atlas, we studied the morphology of the left and right superior articular facets focusing on a possible bipartition. The bipartition was noted as present only if it was complete with two welldefined facets separated by a clear non-articular groove or area; the partial forms were not recorded. This bipartition was sometimes present on both sides, present only on the right side, present only on the left side, or absent.
Results In humans, bipartition of one or both of the superior articular facets of the atlas was observed in 104 individuals out of the 500 in the present
ARTICLE IN PRESS Bipartition of superior facets of the atlas
81
series (20.8%) (detailed results in Table 1). Bilateral occurrence (symmetric manifestation) was observed in 46.2% of the bipartitions and unilateral occurrence in 53.8%. No significant right or left predominance was observed in the frequency of lateral occurrence even if bipartitions were slightly more numerous on the right side (detailed results in Table 2). When a bipartition existed, the morphology of each of the two facets was variable: circular or elliptical; however, in most cases the ventral facet was more or less elliptical and the dorsal facet quite circular. The sizes of the facets were also variable: in some cases the ventral and dorsal facets presented similar sizes, in some cases the
Figure 2. Bilateral bipartition of the superior articular facets of the human atlas, with an elliptical anterior facet and a circular posterior one (superior view).
Table 1. Individual occurrence of bipartition of the superior articular facets in the 500 human atlases of the present series Bipartition
Bilateral Unilateral Left Unilateral Right Total
Number of cases
Frequency (%)
Relative frequency (%)
48 23 33
9.6 4.6 6.6
46.2 22.1 31.7
104
20.8
100.0
Table 2. Side occurrence of bipartition of the superior articular facets in the 500 human atlases of the present series Bipartition Left side Right side Total
Number of cases
Figure 3. Right unilateral bipartition of the superior articular facets of the human atlas, with an elliptical anterior facet and a circular posterior one (superior view).
Frequency (%)
71 81
14.2% 16.2%
152
15.2%
ventral facet was slightly smaller and in others slightly greater. The non-articular area or groove separating the two facets in bipartite cases was situated quite transversally around the middle part of the entire articular area and corresponded to the strangled part of the classical unique facet. The non-articular area was rough and at a deeper level than the articular facets (Figs. 1–3). In non-human primates, no case of bipartition of the superior articular facets of the atlas was found in any of the 256 individuals studied.
Discussion Figure 1. Superior articular facets of the human atlas. Classical reniform or kidney-shaped aspect of both left and right facets with a constriction or strangled part at their mid-length (superior view).
Occurrence of bipartition in humans Precise data concerning the frequency of the bipartition of the superior articular facets of the
ARTICLE IN PRESS 82 Table 3.
F. Billmann et al. Frequency of bipartition of the superior articular facets of the atlas in the main series of the literature
Authors
Number of cases
Number of bipartition
Frequency of bipartition (%)
Dubreuil-Chambardel (1921) Gottlieb (1994) Hasebe (1913) Le Double (1912) Macalister (1893) Poirier (1896) Prescher (1997) Singh (1965) Tsusaki (1924) Present series
Approx. 500 30 100 500 – 500 200 200 22 500
– 7 0 – – – 28 19 2 104
16.0 23.3 0.0 6.1 5.7 Approx. 10.0 14.0 9.5 9.1 20.8
Dash (–): number not precised in the original study.
Table 4. Individual occurrence of bipartition of the superior articular facets of the atlas in the main series of the literature
Table 5. Side occurrence of bipartition of the superior articular facets of the atlas in the main series of the literature
Authors
Authors
Left
Right
5 (16.7%) 13 (6.5%) 13 (6.5%) 71 (14.2%)
4 (13.3%) 24 (12.0%) 9 (4.5%) 81 (16.2%)
Gottlieb (1994) Le Double (1912) Macalister (1893) Prescher (1997) Singh (1965) Present series
Bilateral
2 (28.6%) – (57.4%) – (52.6%) 9 (32.1%) 3 (15.8%) 48 (46.2%)
Unilateral Left
Right
Gottlieb (1994)
3 (42.8%) – – – – 4 (14.3%) 10 (52.6%) 23 (22.1%)
2 (28.6%) – – – – 15 (53.6%) 6 (31.6%) 33 (31.7%)
Prescher (1997)
Dash (–): number not precised in the original study.
human atlas are scarce; the data of the main series of the literature are given in Tables 3–5. There are no data available which specify variations of this bipartition according to sex or age; however, on the whole, the results obtained on the existence of differences in the incidence of expression of other non-metrical traits between males and females, or at various ages, are either negative or show little consistency (Hauser and De Stefano, 1989). Geographical origin could be a factor of intraspecific variation of the frequency of bipartition within human populations even if most series available are based on European individuals. The frequency of bipartition seems to be similar in Indian (Singh, 1965), Formosan (Tsusaki, 1924), and European populations (Table 3). Bipartition seems to be rarer or even absent in Japanese populations as suggested by the absence of any case of bipartition in the 100 individuals studied by Hasebe
Singh (1965) Present series
(1913). For other non-metric variants of the human atlas, and in particular for the bony ponticles over the groove for the vertebral artery, particularities in the frequencies also seem to exist in Japanese populations (review in Le Minor and Trost, 2004). Characterization of a trait as simply present or absent ignores a wider range of variation, which corresponds to the biological reality of variable degrees of expression of traits (Hauser and De Stefano, 1989). However, the difficulty in defining transition types is a source of confusion, and the resulting lack of reproducibility between observers leads to difficulty in comparing data sets (Finnegan, 1978). This is why we decided to consideronly the complete bipartition of the superior articular facets of the atlas as being present; further attempts should be made to determine how to reliably quantify partial forms. When scoring bilateral non-metrical traits three different modes of approach exist (Trinkaus, 1978; Green et al., 1979; Korey, 1980; Hauser and De Stefano, 1989). In the first approach, each of the two sides are scored separately, taking into account bilateral as well as unilateral occurrence; this allows for the determination of side incidence as
ARTICLE IN PRESS Bipartition of superior facets of the atlas well as individual incidence, and for identification of asymmetry of expression. In the second approach, the two sides are scored separately, without taking into consideration the trait on the other side; this allows for the determination of side incidence only. In the third approach, the traits are scored by individuals, only indicating whether the individual shows the trait or not; this allows for the determination of individual incidence only. The choice of sampling by individuals or by sides is most frequently dictated by the exigencies imposed by the fragmentation of the material. We used the first approach, which gives the fullest information; it is, however, easier for an axial structure such as the atlas vertebra in which left and right structures are located on the same bone. The frequency of bilateral occurrence of a trait is generally higher than the frequency expected if combinations of left- and right-sided expressions occurred only at random (independence of the two sides) (Trinkaus, 1978; Green et al., 1979; Korey, 1980; Hauser and De Stefano, 1989). In the case of the bipartition of the superior articular facets of the atlas, very few data are available in the literature concerning its symmetry; the frequency of bilateral occurrence varies between 15.8% and 57.4% according to the series (main results in Table 4). The expression of the bipartition on the left and right sides appear thus to be linked; however, in total, the frequency of asymmetrical occurrences is similar to symmetrical ones or even predominant. Laterality is the tendency of a unilaterally expressed trait to occur more frequently on one side than on the other. In most non-metric cranial traits, there is no convincing evidence of consistent laterality (Hauser and De Stefano, 1989). In the case of the bipartition of the superior articular facets of the atlas, the present study demonstrates similarly that no substantial difference exists between left (14.2%) and right (16.2%) occurrences (Table 2); the rare data in the literature are controversial (Table 5). A tendency to have larger facets on the right side than on the left side has been observed by Mysorekar and Nandedkar (1986) who measured their area in 103 atlases.
Occurrence of bipartition in non-human primates The observations of the present study suggest that the bipartition of the superior articular facet of the atlas does not exist in non-human primates. This also seems to be supported by the data of the literature which are, however, very poor and vague on this trait (Schultz, 1955, 1961; Hartman and
83 Straus, 1933; Olivier and Laffont, 1964; Ankel, 1967; Lessertisseur and Saban, 1967). The main difference between apes and modern humans seems only to consist in superior atlantal facets which are more concave in apes (Aiello and Dean, 1990).
Evolutionary and functional significance From a phylogenetic point of view, a single superior facet of the atlas seems to be the primitive pattern or plesiomorphy in primates as suggested by the comparative data. Modification of this general pattern seems to occur only in some individuals in H. sapiens within primates, and the bipartition of the facet could thus be interpreted as a derived characteristic restricted to the human species or autapomorphy. It is tempting to interpret the appearance of the bipartition of the superior articular facet of the atlas during human evolution as the result of functional modifications due to the acquisition of constant erect posture and bipedalism. The relationships between the evolution of hominoid posture and the positions of the foramen magnum and the occipital condyles have been widely studied (Schultz, 1955; Dean and Wood, 1981, 1984; Aiello and Dean, 1990; Luboga and Wood, 1990; Ahern, 2005). An antero-inferiorly positioned and vertically orientated foramen magnum has been considered linked to erect posture and bipedalism and thus specific to fossil and modern H. sapiens. This forward placement of the foramen magnum in humans has been interpreted as an essential adaptation to balance the head more efficiently on a vertical and erect spine; it has clearly had an effect upon the forces required to move and balance the head and there have been accompanying changes to the cervical muscles. In this context, the constraints in the human atlanto–occipital joint have obviously been modified and the bipartition observed in some individuals could be the reflection of these modifications. A similar bipartition has been described for the human occipital condyles; further studies would be necessary to ascertain whether the bipartitions of the occipital and atlantal facets are always linked (Berry and Berry, 1967; Hauser and De Stefano, 1989). Greater pressures on the anterior and posterior portions of the facet have been proposed by some authors as being the functional factors at the origin of the bipartition (Singh, 1965; Tillmann and Lorenz, 1978). Two roughly circular pressure facets are indeed present and evident in many individuals
ARTICLE IN PRESS 84 in the anterior and posterior parts of the superior articular facets of the atlas even in atlases which show no signs of division; in some cases these are so marked that the rest of the articular area looks non-articular (Singh, 1965). Tillmann and Lorenz (1978) suggested that the bipartition of the corresponding occipital facets in human adults is not controlled genetically, but has an individual mechanical causality and is due to stresses in the postnatal years. Considering the regular shape of the bipartite facets and the regular aspect of the subchondral bone, we suggest, on the contrary, that the bipartition is under genetic control and is the result of a phylogenetic process during which only the articular area submitted to mechanical stresses remains, the area less subjected to mechanical strain tending gradually to become non-articular. The significance of unilateral occurrences or asymmetric manifestations (42.6–84.2% according to the series; Table 4) versus bilateral occurrence or symmetric manifestation could simply be the reflection of a general rule for rare or inconstant traits for which a predictable relationship exists between the frequency of non-metric traits and the probability that they are expressed bilaterally as already demonstrated for cranial non-metric traits (Hallgrimsson et al., 2005). Thus, unilateral occurrences are probably not purely the reflection of asymmetric mechanical constraints. Such unilateral occurrences are similarly observed for all other non-metric traits of the human atlas such as ponticles (Le Minor, 1997; Van Roy et al., 1997; Le Minor and Trost, 2004). The frequent asymmetry in the disposition of the superior articular facet of the atlas probably implies functionally that true symmetry of segmental movement may not be possible in corresponding individuals and is not pathological but only a normal variant; this is of interest for the design of certain chiropractic theories and/or techniques which rely on symmetry as being normal (Van Roy et al., 1997).
Acknowledgment We particularly thank Miss Kate Welch for her help in checking the English language.
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