# Natural History Review/Series 2/Volume 1/Number 2/On the Serial Homologies of the Articular Surfaces of the Mammalian Axis, Atlas, and Occipital Bone

[Read before the Royal Physical Society of Edinburgh, Nov., 1860.]
In works on human anatomy it has been customary to compare the articular surfaces of the atlas, and the superior articular surfaces of the axis, with those of the oblique processes of other vertebræ, as if they were homologous, notwithstanding the apparently anomalous manner in which, according to that view, the first and second spinal nerves must be considered as emerging from the spinal canal. The circumstances which have led to this comparison being made, are merely the rapid diminution in size of the intervertebral discs from the thoracic region up to the axis, and a general similarity of appearance between the articular surfaces of the atlas and axis and those of succeeding vertebræ: and though the impropriety of this comparison has been exposed in very explicit terms by Prof. Henle, there is still room for a few remarks as to the precise parts of other vertebrae to which the surfaces in question correspond.
In order to arrive at a just conclusion upon this subject, we shall find it advantageous to examine the atlas in the bird. In it we find on the posterior aspect a pair of true oblique processes passing backwards, to articulate above the intervertebral foramina with a corresponding pair of processes of the axis, similar to those of succeeding vertebræ; while inferiorly there is a cartilaginous surface which forms, with the body of the axis and its odontoid process, a joint similar to those between the succeeding bodies of vertebræ. On the anterior aspect of the ​atlas there are no articular processes like the posterior pair; and there is presented for articulation with the condyle of the occipital bone, a single surface, exactly corresponding in extent with that which articulates with the body of the axis. As regards the occipital condyle, its constitution will be best understood by looking at the quite similar condyle of the occipital of the turtle. In it the middle and lower portions are formed by the basi-occipital, in precisely the same manner as the body of a vertebra is formed principally by the centrum, but has its superior angles derived from the arch. Thus, there can be no doubt that the atlo-occipital articulation in birds, as well as the inferior atlo-axoid articulation, belongs to the same series as those between the bodies of the succeeding vertebræ.
It remains for us to show that they also correspond to the atlo-occipital and atlo-axoid articulations in mammals: and that they do so will readily appear, on making a more careful examination of the anterior articular surface of the atlas of the bird in the recent condition. It presents the form of a cup perforated by a small foramen, through which a ligament passes from the tip of the odontoid process to the occipital condyle, and the part of the cup which lies above the foramen is formed by a transverse ligament. This transverse ligament corresponds to those which pass from side to side of the bodies of other vertebræ and are attached to the superior angles of their anterior aspects—those angles which are derived from the arches. Now, in mammalia, not only is the function of the tranverse ligament of the atlas the same as in birds; but in many of them the heads of the ribs of opposite sides are united above the intervertebral discs by transverse ligaments (ligamenta conjugalia costarum), which very obviously correspond to the ligaments just mentioned on the vertebrae of the bird; for, though they do not, like them, pass from angle to angle of the bodies of the vertebræ, they are attached to structures interpolated between these angles. It appears, therefore, that the transverse ligaments of the atlas and other vertebræ in birds, and the ligamentum conjugale costarum, and transverse ligament of the atlas in mammals, are all homologous structures: and, in that case, the only difference between the atlo-occipital articulation in the mammal and in the bird is, that while in the latter it is single, in the former it is divided into two lateral parts. But this is not an important distinction; for in the atlo-axoid articulation, we find the arrangement in many mammals, as in the human subject, similar to that of the atlo-occipital; while in others, as in the sheep, a single joint extends across the middle line exactly as in the bird.
The serial correspondences of the vertebral articulations are very well illustrated in the human fœtus. The articular surfaces of the oblique processes are situated immediately behind the transverse processes, and ​in the cervical region the arches are bulged outwards at the points where they are placed (Fig. 5). The axis is shaped altogether like one of the succeeding vertebræ, except only that the odontoid process is super-added to the centrum: and the bulging of the arch on each side behind the transverse process is well marked, and bears the inferior articular surface on its under side. On the other hand, the superior articular surface is placed partly on the odontoid process, but principally on the most anterior part of the arch, viz. that part which, in all the succeeding vertebræ, forms the posterior angle of the body (Fig. 3). So also on the anterior extremity of the arch are placed the articular surfaces (both superior and inferior) of the atlas (Fig. 4); and also, in the dorsal region, the surfaces for the heads of the ribs. The occipital condyles are placed upon the most anterior parts of the arch of the occipital bone, and to a small extent upon the centrum.
The foregoing examination of vertebral articulations leads us to observe, that, when surfaces for a synovial joint are present upon the body of a vertebra, however little of the body they may cover, they are never absent from those angles which are formed by the arches.
The synovial articulations between the bodies of vertebræ in mammals are arranged in the following manner: In the dorsal region are the synovial capsules for the heads of the ribs, which always occupy the angles of the bodies, but are also, in many animals, united across the middle line between the intervertebral disc and the conjugal ligament; while in some cases, as in the horse and the sheep, a small line of cartilage is stretched along the superior margin of the posterior of the two vertebræ concerned in each joint. In the cervical region in the human subject, the minute joints described by Luschka, are situated between those parts of the bodies which are formed by the arches. Lastly, in the atlo-axoid and atlo-occipital articulations, the principal parts of the articular surfaces are placed upon those parts of the arches which correspond to the angles of the bodies of succeeding vertebræ, while the intervertebral discs have disappeared.
I may here remark that, if the odontoid process be regarded as the centrum of the atlas,—a view which seems to be supported by its very large comparative size in the young condition, long before the anterior tubercle of the atlas makes its appearance—then we must recognise in the odontoid ligaments the terminal member of the series to which the transverse ligament of the atlas and the ligamenta conjugalia belong: and indeed the arrangement of their fibres, some of which are continuous from side to side, is favourable to this supposition, and reminds one of the ligamentum conjugate in the sheep.
Note.—Since writing the above, my attention has been called to Rathke's work "Ueber die Entwickelung der Schildkröten," in which (page 77), the view that the odontoid process is the centrum of the atlas is strenuously urged, and strong evidence brought forward in its favour. ​See also "Owen, On the Homologies of the Vertebrate Skeleton," page 93. Rathke points out that the ligamentum suspensorium, which, in the birds and higher reptilia unites the odontoid process to the occipital condyle, is the serial representative of the intervertebral discs behind. He found that in most chelonians it consisted of true cartilage, and that in certain birds it was composed of fibro-cartilage. This view of the ligamentum suspensorium is quite consistent with the suggestion which I have offered, that the ligamenta alaria are homologous with the transverse ligament.
The large portion of the cup on the anterior aspect of the chelonian atlas, which is formed by the expanded inferior extremities of the arch, illustrates very well the unity of plan upon which the articular surfaces of the atlas are formed in animals having one occipital condyle, and those which have two. This will be seen by comparing the woodcuts below.
When, in the human subject, a process of bone passes up from the arch of the atlas, to meet the superior articular surface and convert the groove for the nerve and vertebral artery into a foramen, the process in question is a true oblique process. If, in addition, we were to imagine the tip of the transverse process thickened and projecting upwards to meet the superior articular surface, we should then have presented to us the condition of parts found in the pig and the sheep.
Fig. 1 . Atlas of a young Chelonia virgata—after Rathke. a. The arch. b. Osseous centre of the tubercle.
Fig. 2. Dorsal vertebra of a young seal, for comparison with the following figures: a. Oblique process. b. Articular surface for head of rib.
Fig. 3. Superior aspect of the axis of a human fœtus, a. The centrum, b. Odontoid process, c. Superior articular surface, d. Bulging of the arch in the situation of the inferior articular surface.
Fig. 4. Inferior aspect of the atlas of the same subject, a. Articular surface.
Fig. 5. Cervical vertebra from the same subject, a. Oblique process, b. Part of the arch entering into the composition of the body of the vertebra.
* ↑ Henle, Handbuch der Syst. Anat. des Menschen, I., p. 42.
* ↑ I have described and figured the ligament here referred to in a paper "On the Structure, Actions, and Morphological Relations of the Ligamentum Conjugale Costarum," in the Edinburgh New Philosophical Journal, April, 1859.
* ↑ Luschka, Die Halbgelenke des Menschlichen Körpers, 1858, p. 71, and Tab. I., fig. 1.