J. Anat. (1984), 138, 2, pp. 259-266 259 With 9 figures Printed in Great Britain The ossification of the membranous part of the squamous occipital in man G. P. PAL, B. P. TAMANKAR, R. V. ROUTAL AND S. S. BHAGWAT Department of Anatomy, Government Medical College, Surat 395001, Gujarat, India (Accepted 30 June 1983)

INTRODUCTION The interparietal part of the squamous above the highest nuchal line develops in membrane. Ranke (1913), in his account of the development of the membranous part of the squamous occipital bone, describes two pairs of centres and an occasional third pair (pre-interparietal) at the upper angle of the bone. Both Brash (1951) and Breathnach (1965) have also described the pre-interparietal centres in addition to the interparietal centres. Srivastava (1977), on the basis of anomalies observed in a large number of , confirms the three pairs of centres described by Ranke (1913). Warwick & Williams (1980) state that the membranous part of the occipital bone consists of two elements, interparietal and pre-interparietal. Both Srivastava and Warwick & Williams also consider that a separate boneatthe posterior () may represent the pre-interparietal element. However, they do not rule out the possibility of sutural bone formation at the lambda. The aim of the present study is to differentiate the true pre-interparietal bone from the sutural at the lambda.

OBSERVATIONS A total of 348 apparently normal skulls was examined from the collections of one dental college and three medical colleges of Gujarat State. Various anomalies in the interparietal region were found: a single separate interparietal bone in four skulls, a separate central piece of bone in two skulls, two separate pieces (a central and a right lateral) in one and three separate pieces (one central and two lateral) in two skulls (Figs. 1-4). A triangular piece of bone behind the lambda occurred in two skulls (Figs. 5, 6). A suture separating this triangular piece of bone ran transversely, approximately in the middle of the interparietal part, extending from one side of the lambdoid suture to the other. The ends ofthis suture were upturned near its junction with the lambdoid suture, though this was not well marked in one skull (Fig. 5). In one skull (Fig. 5) this suture was situated 4-8 cm above the external occipital protuber- ance and 3-5 cm below the lambda, while in the other skull (Fig. 6) it was situated 3-8 cm above the external occipital protuberance and 3-4 cm below the lambda.

DISCUSSION Ranke (1913) describes two pairs of centres and an occasional third pair at the upper angle of the occipital bone during the ossification of its interparietal part. One pair arises in membrane above the supraoccipital cartilage, each centre extending 9-2 260 G. P. PAL AND OTHERS

Fig. 1. Interparietal-supraoccipital suture separating a complete interparietal bone above the external occipital protuberance and highest nuchal line.

Fig. 2. A separate central piece in the interparietal region is situated above the external occipital protuberance. Membranous part ofoccipital bone 261

Fig. 3. An occipital bone showing two separate bones in the interparietal area, right lateral and central piece, while the left lateral piece is fused with the occipital bone.

Fig. 4. Interparietal area showing three independent bones, a central piece and two lateral plates. 262 G. P. PAL AND OTHERS

Fig. 5. A triangular piece of bone below the lambda is separated from the remaining inter- parietal area by a transverse suture.

Fig. 6. A triangular piece, as in Fig. 5, showing upturned ends of the transverse suture. Membranous part ofoccipital bone 263 upwards and laterally to form a lateral plate of bone. A second pair ofcentres appears between the two lateral plates, one centre on either side of the mid-line, and fuse to form the remainder of the interparietal bone (central portion). Failure of fusion between these two pairs of centres and with those of the supraoccipital can give rise to the various anomalies in the interparietal area. Thus, a separate interparietal bone (Fig. 1) can result from the fusion of both pairs of centres in membrane and its failure to fuse with the supraoccipital at the level of the highest nuchal line. A central piece (Fig. 2) is obtained when the second pair of centres fail to unite with the lateral plates at the sides and the supraoccipital below. Sometimes, a fused lateral plate and central piece are separate, with the other lateral plate fused with the supraoccipital (Fig. 3). Two lateral plates and one central piece can persist as three independent bones (Fig. 4) when the two pairs of centres fail to unite with each other and with the supraoccipital below. If the pair of centres for the central piece fail to unite with each other or with the lateral plates, the interparietal may develop as two symmetrical halves (Brash, 1951), or as four pieces. Srivastava (1977), on the basis of anomalies observed in a large series of skulls, confirms the two pairs ofcentres described by Ranke (1913). The present findings are similar to those of Srivastava, and confirm the presence of a pair of centres for the two lateral plates and a pair for the central piece. In addition to the two pairs of centres already discussed, Ranke (1913) describes an occasional third pair of centres for the ossification of the membranous part of the occipital bone, which may develop at the upper angle of the bone. Similarly, Breathnach (1965) describes additional centres (pre-interparietal) appearing anterior to the interparietal centres. In about 3 % of skulls, Srivastava (1977) finds a separate bone present at the lambda, in the posterior part of the . He considers these bones to be pre-interparietal bones developed from the occasional pair of centres described by Ranke (1913) and by Breathnach (1965). Warwick & Williams (1980) believe that the membranous part of the bone above the highest nuchal line consists of two elements, an interparietal and a pre-interparietal. They also consider that a separate bone in the position of the (lambda) may repre- sent a pre-interparietal element. However, neither Srivastava (1977) nor Warwick & Williams (1980) rule out the possibility of sutural bone formation at the lambda. It is considered, for the reasons given below, that these bones present at the lambda (anterior to the interparietal, in the posterior part of the sagittal suture) are true sutural bones and should not be regarded as bone developed from the pre- interparietal centres described by Ranke (1913). An occasional pair of centres for the pre-interparietal bone appears above the interparietal centres at the upper end of the membrane which develops into the future interparietal bone (Fig. 7). These centres (pre-interparietals) fuse with the bone formed by the interparietals (Breathnach, 1965). Hence, it is considered that whenever occasional pre-interparietal centres appear, ossification of the mem- branous part of the squamous occipital bone is completed by all three pairs of centres. Thus a central piece (Fig. 2) is formed by two pairs of centres, the lower part by the second pair and the upper part by the third pair (pre-interparietal). The first pair will form the areas of the two lateral plates as usual. In the absence of pre- interparietal centres the whole of the central piece is formed by the second pair of centres. The pre-interparietal centres being situated in the membranous primordium of the interparietal bone, they cannot contribute to the occipital bone outside its limits, i.e. anterior to the superior angle, as claimed by Srivastava (1977). They 264 G. P. PAL AND OTHERS

Fig. 7. Skull showing an ossicle at the lambda.

5

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41'

B Fig. 8. Development of the occipital bone (After Sappey, 1876). Fetus of three months. 1, basi- occipital; 2, occipital laterale; 3, condyle; 41, occipitale superius; 4', interparietale; 5, preinterparietale; 61 cartilage; 6', membranous portion of occipital. . Membranous part ofoccipital bone 265

1.5 4 5 - Fig. 9. Diagram obtained after superimposition of ossicles of skulls 4 and 6. 1, lateral plate; 2, lower half of central piece; 3, upper half of central piece; 4, external occipital protuberance; 5, superior nuchal line. should form bone within the interparietal area. If this were not the case, fusion ofthe centres of the pre-interparietal, anterior to the superior angle, with centres for the the central piece, would give an abnormal irregular rounded or tongue shaped upper end of the squamous occipital bone projecting into the posterior part of the sagittal suture. No such bone has been found. The contention that bone formed by pre-interparietal centres should be confined within the limits of the interparietal area of the occipital bone is based on the evidence of an anomaly found in two skulls (Figs. 5, 6). Here a transverse suture is found in the middle of the central part of the interparietal area dividing it into two unequal portions, namely, upper triangular and lower quadrangular parts. The upper triangular piece, forming the superior angle and the adjacent area of the interparietal bone, is situated behind the lambda within the limits of the interparietal bone. If the interparietal areas of Figures 4 and 6 are superimposed, four roughly triangular pieces of bone are obtained (Fig. 9). The first pair of centres give two lateral plates, the second pair of centres give the lower ossicle of the central area and the third pair (pre-interparietal) give an upper piece of triangular bone behind the lambda. Thus, it becomes evident that an ossicle like that in Figures 5 and 6 can be found only when there is a failure of fusion between the second and third pair (pre-interparietal) of centres. Hence, a separate pre-interparietal bone should be defined only when it is present behind the lambda within the territory of the membranous part of the occipital bone and is separated from the remaining interparietal part by a suture. It should be differentiated from sutural bones at the lambda by its shape and position (Figs. 5, 6). All other ossicles present at the lambda but at the posterior part of the sagittal suture, as shown in Figures 4 and 7, should be dismissed as sutural bones. As pre-interparietal centres are only occasional centres, their failure of fusion with the second pair of centres and the resulting separate pre-interparietal bone would be extremely rare. Srivastava (1977) reports separate interparietals in less than 0-5 % of skulls yet finds pre-interparietal bones in about 3 % of skulls. It is apparent that 266 G. P. PAL AND OTHERS sutural bones are being termed pre-interparietal bones. The anomaly found in the present study (Figs. 5, 6) has not been reported previously and was not observed by Srivastava. This has misled Srivastava (1977) and Warwick & Williams (1980) to consider ossicles at the lambda as pre-interparietal bones. The name 'pre-interparietal', given to the bone developed from this occasional pair of centres and found as a separate piece, is misleading and its use should be discontinued. The bone may be referred to as the upper central piece of the inter- . SUMMARY The membranous part of the squamous occipital bone, above the highest nuchal line, develops from two pairs of centres and an occasional third pair, pre-inter- parietal, which may develop anterior to the interparietal centres. Previously it was considered that the pre-interparietal bone is found at the lambda, anterior to the interparietal, which is also a common site for the formation of sutural bones. In this study, on the basis ofanomalies observed in a large series ofskulls, sutural bones at the lambda are differentiated from the bone developed from the pre-interparietal centres. A separate pre-interparietal bone is identified by its shape and position. It is present behind the lambda within the territory of the membranous occipital bone.

REFERENCES BRASH, J. C. (1951). In Cunningham's Text Book of Anatomy, (ed. G. J. Romanes), 9th ed. p. 220. London: Oxford University Press. BREATHNACH, A. S. (1965). In Frazer's Anatomy ofthe Human Skeleton, 6th ed., p. 190. London: J. & A. Churchill. RANKE, J. (1913). Cited by E. A. Schafer, J. Symington & T. H. Bryce (1915) in Quain's Elements of Anatomy, 11th ed., vol. iv, part 1, pp. 53-55. London: Longman, Green & Co. SAPPEY, Ph.C. (1876). Cited by F. KEIBEL & F. P. MALL (1910) in Manual of Human Embryology, vol. 1, p. 425. Philadelphia and London: J. B. Lippincott Co. SRIVASTAVA, H. C. (1977). Development of ossification centres in the squamous portion of the occipital bone in man. Journal ofAnatomy 124, 643. WARWICK, R. & WILLIAMS, P. L. (1980). In Gray's Anatomy, 36th ed., pp. 338 and 322. Edinburgh: Longman.