J. Anat. (1977), 124, 3, pp. 643-649 643 With 7 figures Printed in Great Britain

Development of ossification centres in the squamous portion of the occipital in man

H. C. SRIVASTAVA Department of Anatomy, Medical College, Baroda, India. (Accepted 15 October 1976)

INTRODUCTION The squamous portion of the in man consists of an interparietal part which lies above the nuchal lines and ossifies in membrane, and a supraoccipital part which develops in cartilage and is situated between the nuchal lines and the posterior margin of the . The interparietal may exist as separate, symmetrical halves, or it may be in three pieces - or even four, in which case the upper two constitute the pre-interparietal (Brash, 1951). Misra (1960) has reported a with a separate interparietal bone. Kolte & Mysorekar (1966) have described a tripartite interparietal bone. Keith (1948) stated that a separate single interparietal bone in man is an extremely rare anomaly. No other anomalies of the interparietal, nor any anomaly of the supraoccipital, are mentioned in the literature. Analysis of the anomalies of the occipital bone reported in this paper has resolved differences between authors regarding ossification centres in the squamous portion, and also regarding the precise limits of the interparietal and supraoccipital.

OBSERVATIONS A series of 620 human was examined for anomalies in the squamous portion of the occipital, and 25 such were found. These are illustrated and described from the following representative specimens. Skull no. 1. A single separate interparietal is seen (Fig. 1). The suture between the interparietal and supraoccipital lies 2 cm above the external occipital protuberance and 0 4 cm above the superior nuchal line near the lambdoid suture. A sutural bone is present in the right lambdoid suture. Skull no. 2. A separate bone is present in the middle of the interparietal, leaving two nearly equal triangular areas on each side which are fused with the supra- occipital (Fig. 2). The sutures between this separate bone and the remaining bone extend from a point 2-3 cm above the external occipital protuberance in the midline to the lambdoid suture on each side. A line drawn in the central plane through this bone divides it into two more or less equal triangles. Skull no. 3. A large separate bone forms the left three fourths of the interparietal, with the right one fourth represented by a triangular area which is fused with the supraoccipital. The former is separated from the rest of the bone by a suture which begins like the interparietal-supraoccipital suture from the left lambdoid suture and extends to the midpoint 2-6 cm above the external occipital protuberance. From this point it runs obliquely upward and laterally through the interparietal region to join the right lambdoid suture near its middle. If from the above midpoint the left interparietal-supraoccipital suture is extended similarly on the right side, and 644 H. C. SRIVASTAVA

Fig. 1. Complete separate interparietal bone. The superior and highest nuchal lines are below the interparietal-supraoccipital suture. Fig. 2. Shows a separate central piece in the interparietal region. The external occipital pro- tuberance and superior nuchal line are below it. the oblique suture is drawn to the left lambdoid suture, the interparietal part is divided into three parts - i.e. right and left triangular areas of similar shape and size and a central piece. The central piece resembles the separate bone described in skull no. 2. The superior and highest nuchal lines are below the interparietal- supraoccipital suture, which is 03 cm above the former line near the lambdoid suture. Small sutural are present in the lambdoid sutures. Skull no. 4. The interparietal is represented by three independent bones articu- lating with each other and with the supraoccipital by sutures. Right and left tri- angular plates are symmetrical mirror images (Fig. 4). The central piece resembles the separate bone seen in skull no. 2, and the right and left triangular plates corres- pond to the triangular areas drawn in skull no. 3. The superior and highest nuchal lines are below the three bones. The suture between these three separate bones and the supraoccipital part is 1 1 cm above the external occipital protuberance and 05 cm above the superior nuchal line near the lambdoid suture. Small sutural bones are seen in the lambdoid suture on both sides. Skull no. 5. The interparietal is a single bone. It is separated from the supra- occipital by a suture on the right side and by a suture and a gap on the left side (Fig. 5). The gap is 3-7 cm in length, its maximum width is 0O8 cm and it starts 05 cm to the left of the external occipital protuberance, ending 1-3 cm from the lambdoid suture. The superior nuchal line is seen below the interparietal-supra- occipital suture on the right side. Examination of the internal aspect of the skull shows a well marked internal occipital protuberance, and the groove for the trans- verse sinus lies above the gap on the left side and at the interparietal-supraoccipital suture on the right side. The supraoccipital consists of central, right and left segments. The central segment is separated from the right and left portions by right and left vertical sutures which extend from the interparietal-supraoccipital suture to the posterior margin of the foramen magnum 1-5 cm on each side of the midline. The left vertical suture presents small gaps in its upper portion. Its lower portion is obliteratedjust above the foramen magnum, but its position is marked by a groove. The right vertical suture is distinct Ossification centres in the occipital bone 645

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Fig. 3. Three fourths of the interparietal forms a separate bone. The suture between this separate bone and the rest of the bone begins from the left lambdoid suture and extends to the midpoint above the external occipital protuberance. From this point it runs obliquely upwards and laterally through the interparietal region to the right lambdoid suture. Superior and highest nuchal lines are distinctly seen below the suture. Fig. 4. The interparietal bone is replaced by three independent bones. The right and left tri- angular plates appear as mirror images.

Fig. 5. Shows a separate interparietal and a small pre-interparietal anterior to it. The inter- parietal-supraoccipital suture presents a big gap on the left side. The supraoccipital part shows right and left vertical sutures separating the right and left segments from the central segment. Fig. 6. Inferior view of the skull seen in Fig. 5 shows superior horizontal sutures at the level of the inferior nuchal line dividing the right and left segments into superior and inferior pieces, and inferior horizontal sutures behind the posterior condylar fossae. The lower part of the right vertical suture extends to the posterior margin of the foramen magnum. 646 3H. C.7 SRIVASTAVA~~~~~~~~~~~~8 'b.~~~~~~1

Fig. 7. Diagram showing the occipital bone of skull no. 5. 1, pre-interparietal; 2, interparietal; 3, left vertical suture; 4, left superior horizontal suture; 5, left inferior horizontal suture; 6, interparietal-supraoccipital suture; 7, superior nuchal line; 8, right vertical suture; 9, right superior horizontal suture; 10, inferior nuchal line; 11, right inferior horizontal suture. in its entire length and presents a small gap 1 8 cm above the posterior margin of the foramen magnum. The central segment forms more than half the posterior margin of the foramen magnum. The right and left segments articulate laterally with the inferior angle of the and the mastoid part of the , medially with the central segment, superiorly with the interparietal bone, and inferiorly with the condylar part of the occipital bone at the inferior horizontal sutures which begin near the lower ends of the vertical sutures and run laterally behind the posterior condylar fossae (Fig. 6). The inferior horizontal suture is marked on the left side by a gap in the middle and a groove on either side, while on the right side it is seen as a faint groove. The right and left segments are incompletely divided into upper and lower pieces by superior horizontal sutures situated at the level of the inferior nuchal lines (Fig. 7). These sutures are present medially near the vertical sutures, but are obliterated laterally. A small pre-interparietal bone, 1-3 cm long and 1-2 cm wide, is present anterior to the interparietal in the posterior part of the sagittal suture. From a study of 620 skulls a pre-interparietal was seen in 18 skulls, a complete separate interparietal in 3 skulls, a separate bone in the middle region of the inter- parietal part in 2 skulls, and the remaining anomalies reported each in 1 skull. No signs of injury or of any pathological condition were seen in the squamous portion of the occipital bone in any skull. Ossification centres in the occipital bone 647

DISCUSSION The usual textbook description of the ossification of the squamous portion of the occipital bone is that, above the highest nuchal line, it is ossified in membrane from two centres, one on either side of the midline. These form the interparietal part, and may remain separate throughout life. Below the highest nuchal line, the squamous part is ossified in cartilage from two centres which soon unite to form a single piece. An occasional centre appears in the posterior margin of the foramen magnum (Warwick & Williams, 1973). Keith (1948) described the part of the occipital bone above the superior curved (nuchal) lines as developing by four centres of ossifi- cation in membrane, this membranous part constituting the interparietal bone. Ranke (1913) described three pairs of centres, and an occasional fourth pair at the upper angle of the bone. The first pair appear in the cartilage rudiment of the supraoccipital, and give rise to the whole of the element, except a strip along the upper margin. The second pair arise in membrane above the supraoccipital cartilage, each centre extending upwards and laterally to form a lateral plate of bone. The lower part of this plate of bone becomes fused with the supraoccipital to form its upper margin, while the upper part constitutes the greater part of the interparietal. The pars interparietalis is completed by another plate of membrane bone, which arises from the fusion of a third pair of centres between the lateral plates. According to Keibel & Mall (1910) the occipitale superius (squama, inferior part) arises from four centres and the interparietal (squama, superior part) from two centres of ossification. The first centres of ossification to appear are two bilaterally placed centres for the occipitale superius which arise in cartilage immediately dorsal to the foramen magnum. These centres unite across the midline, and are joined by two secondary centres, one of which arises on each side. Occasionally an additional unpaired median centre appears on the dorsal margin of the foramen magnum. The two bilaterally placed interparietal centres appear in the membranous tissue which extends anteriorly from the occipitale superius. These membranous tissues are rectangular in form and unite to form the interparietal bone. Schaeffer (1942) described a membranous space extending from the centre of the squamous portion to the foramen magnum, partially separating the lateral portions of the supra- occipital. This space is occupied later by a spicule of bone (ossicle of Kerckring). Breathnach (1965) described the lower squamous part as developing from one centre, but suggested that there is the possibility that this is initially paired. The inter- parietal apparently begins from paired centres which rapidly become continuous with each other and with the lower squamous ossification. Additional centres occurring anterior to the interparietal, and fusing with it, are known as pre-inter- parietals. The interpretation ofthe evidence presented in this communication is that the inter- parietal develops from two pairs of centres -the second and third pairs described by Ranke (1913). One pair form lateral plates and the other pair unite to form a central piece. If the pair ofcentres for the central piece fail to unite with each other or with the lateral plates, the interparietal may develop as two symmetrical halves or as four pieces. In skull no. 2 the central piece formed by a pair ofcentres has persisted as a separate bone, while in skull no. 3 the central piece and the left lateral plate have fused to form a separate interparietal bone. In skull no. 4 the lateral plates and the central piece have persisted as three independent bones. To this development of 648 H. C. SRIVASTAVA the interparietal bone can be added further centres - an occasional fourth pair at the upper angle of the bone described by Ranke (1913), and additional centres described by Breathnach (1965) as pre-interparietals. A pre-interparietal bone which may have developed from such centres is evident in 18 of the skulls examined, though it is difficult to rule out the possibility of sutural bone formation at the lambda. Kolte & Mysorekar (1966) have suggested that in skulls like no. 4 the three independent bones are sutural bones which have replaced the interparietal bone. However, the present author considers that these bones are normal developmental parts of the interparietal- bone and can be identified as such by their position, size and shape. Keith (1948) has described the- interparietal bone developing from four centres (two pairs) apparently not including centres for a pre-interparietal. The suture between interparietal and supraoccipital lies about 2 cm above the external occipital protuberance, and above the highest nuchal line, and thus the upper margin of the supraoccipital is not contributed by the lower parts, of the lateral plates developing in membrane from the second pair of centres described by Ranke (1913). The supraoccipital develops from two pairs of centres for its right and left seg- ments, and an unpaired centre for the central segment, as described by Keibel & Mall (1910). In skull no. 5 the superior and inferior pieces of the right and left segments, and the central segment, all developing from independent centres, have failed to unite completely with each other. The inferior pieces of the right and left segments evidently develop from centres arising in cartilage immediately dorsal to the foramen magnum, while the superior pieces presumably develop from the two secondary centres. The central segment develops from the additional unpaired median centre; which may correspond to the ossicle of Kerckring mentioned by Schaeffer (1942), or to the occasional centre appearing in the posterior margin of the foramen magnum described by Warwick & Williams (1973). The ossification centres developing in the squamous part of the occipital bone appear to be bilaterally symmetrical and contribute more or less equal parts on each side. It is conceivable that the central segment of the supraoccipital, also develops from a pair of centres which fuse immediately after appearing, though at present there is no evidence in support of this.

SUMMARY The development of ossification centres in the squamous portion of the human occipital bone is described on the basis of anomalies observed in a large series of skulls. The interparietal part develops, from three pairs of centres in membrane - one pair for the lateral plates, one pair for the central piece, and the third pair repre- senting the pre-interparietals. The supraoccipital part develops from five centres in cartilage - two centres for each lateral segment and a single centre for the central segment. The supraoccipital part extends from the posterior margin of the posterior condylar fossae to about 2 cm above the external occipital protuberance and about 0 4 cm above the superior nuchal line near the lambdoid suture. Ossification centres in the occipital bone 649

REFERENCES BRASH, J. C. (1951). In Cunningham's Text Book ofAnatomy, 9th ed., pp. 220. London: Oxford University Press. BREATHNACH, A. S. (1965). In Frazer's Anatomy ofthe , 6th ed., pp. 190. London: J. and A. Churchill. KEIBEL, F. & MALL, F. P. (1910). In Manual of Human Embryology, vol. I, pp. 425-427. London: J. B. Lippincott Co. KEITH, A. (1948). In Human Embryology and Morphology, 6th ed., pp. 223-224. London: Edward Arnold and Co. KOLTE, D. T. & MYSOREKAR, V. R. (1966). Tripartite interparietal bone. Journal of the Anatomical Society of India 15, 96. MISRA, B. D. (1960). Interparietal bone: A case report. Journal of the Anatomical Society of India 9, 39. RANKE, J. (1913). Ober das Interparietale und die Verknocherung des Schadeldaches beim Affen. Cited by E. A. Schafer, J. Symington and T. H. Bryce (1915) in Quain's Elements ofAnatomy, 11th ed., vol. iv, part I, pp. 53-55. London: Longmans, Green and Co. SCHAEFFER, J. P. (1942). In Morris' Human Anatomy, 10th ed., pp. 130. Philadelphia: Blakiston Co. WARWICK, R. & WILLIAMS, P. L. (1973). In Gray's Anatomy, 35th ed., pp. 287-288. Edinburgh: Longman.