GROWTH O F T H E CALVARIA IS T H E RAT

T H E DETERMISATION O F OSSEOL-S 3 I O E P H O L O G T

XINETEEN FIGURES

ISTRODUCTIOS

The growth of the calvaria is an integrated proce>s of

osteogeriesis and of proliferation of tlicl intervening soft
tissues within the originally membranous cranial capsule.
At the onset of ossification each calvarial bone is surrounded
hy a portion of this capsule which separates it from the adja-
cent bones. Any such soft tissue area map be regarded a s
a suture. However, at this early stage, this relatively undif-
ferentiated tissue may properly be called a presumptive su-
ture. The individual bones continue to increase in surface
area during the period of growth until their definitive form
is attained. As this occurs, the individual bones come into
close approximation to each other. The plane of the suture
perpendicular to the vault surface will describe the plane
of articulation between these bones a t the suture. I n the
period of definitive form it is proper to regard this relatively
well differentiated tissue area a s a definitive suture. Througli-
out this developmental process the sutural tissues proper,
together with the peripheral edges of the adjacent bones, are
regarded as the sutural areas.
Consideration of the influence of this sutural growth on
the development of the calvaria presents several prohlems
of major importance. One of these prohlenis is the extent
' Subiiiitted in partial fulfillinent of tlir requirements f o r the degiee of 1)octor
of Philosophy, in the Faculty of Pure Science, Columbia Cniversitp.
Post-Doctoral Fellow, National Institutes of Health.
333
334 nrmvm L. MOSS

to which the shape of ;in individual calvarial bone i q pre-

determined by the location of its sutures. Another problem
is the function of these sutures in the growth of the calvaria.
Theoretical views on these problems are not in agreement.
Traditionally, a calvarial suture is regarded as indicating
the plane of articulation resulting from the growth of the
individual calvarial bones. The csact location of these sutures
is then only the expression of the growth rates in variou-
dimensioiis of these same bones (von Gudden, 1874). Cur-
rently, it is believed that it is the location o f the calvarial
sutures which primarily predetermines the shape o f the indi-
vidual bones of the skull vault (Troitsky, '32). The reestab-
lishment of normal osseous and sutural morphology f ollowiiig
partial and total calvariectomy, in juvenile and adult ani-
mals, reported by Heine (1837) and Simpson et al. ('53),
may be cited in support of this concept.
The role of the suture as a site of gromth is also in dispute.
One group views the suture as a primary site of growth of
the skull, functioning as an "epiphyseal center ' (Mair, '26 ;
Weinmann and Sicher, '47). Another group regards the
suture as only a passive mechanism allowing for relative
movement between the bones of the skull during growth
(Rlijsberg, '32; Brash, '34). I n this view the periosteal tis-
sues are the primary growth sites.
By utilization o f the calvaria of the young, actively growing
rat, an experimental study of some of the factors which
determine the position of the calvarial sutures is possiblc.
The role of the suture as R site of growth in the nioldinq of
the sliull vault may also be critically tested. I n addition, the
relation of these problems to the developmental histology of
the calvaria may be established. As a result of this study,
the opposing views on these problems prove not t o be mutu-
ally exclusive. It is possible t o present an eclectic conciliatioii
between them.
hfA\TERIhLR AND METHODS
I n preliminary experiments with a strain of Long-Evan.
rats, it was observed that when a calvarial bone of an infailtile
 ( ; R O W T H O F THE CALVARTA 1X T H E RAT 335

r a t was removed, together with the periosteal layer of the

underlying dura, regeneration of this bone did not occur.
This observation permitted the study of the effect of this
removal on the morphology of the adjacent groiving bones.
Similarly, it was possible to study the effect of the removal
and subsequent non-regeneration of the calvarial sutures.

Operative procedures ( s e e fig. 1 )

1. Surgical removal of a portion of the parietal bone. One
side of the excised portion bordered the coronal sutnre, the
other three sides lay within the bone.

I 2 3

3 3
Fig. 1 IXagrnininatic representation of oprrativr areas. Cross-liatcliing indi-
cates the approximate area of extirpation. Numerals correspond t o the procedures
ieferred t o in the text.

2. Surgical removal of adjacent portions of both parietal

aiicl frontal bones, including the intervening portion of the
coronal suture.
3. Surgical removal of portions of both parietal bones,
both frontal bones, or all 4 together, including the interven-
ing portions of the sagittal, metopic (interfrontal) and c o ~ o n a l
sut u r e s.
 The area of bone removed in these procedures varied in
amount iii the individual animals from 1 to 5 mm in length,
and froni 1 to Ymni in width.
4. Surgical removal of the various sutures, either singly
or severally.
5. C'auterization of these same sutures.
6. Periosteal scraping and burnishing, often followed by
application of various chemical solutions as described later.
Rats up to 4 days of age were anaesthetized by chilling in
a refrigerator. Ether was administered to the older animals.
The skin over the calvaria was incised parasagittally, the
area exposed and one of the above technics applied. The op-
ei*ative area was always within the essentially flat surface of
the neuro-cranium, well excluded from the site of attachment
of the muscles of mastication. I n the young rat, as the peri-
osteal layer of the dura was not easily separated froni the
overlying bone, simple extirpation was sufficient t o eliminate
regeneration. The exposed dura was not routinely burnished
n-itli cotton. I n a few cases where there was regeneration,
tlic outer osteogenic laycx of the dura had been intentionally
left intact as a result of careful surgical manipulation. The
inner, fibrous layer of the dura was usually left intact. An
owabioiial cerebral herniation was treated by removal of the
herniated mass. Xo ill effects were observed as a result of
t h e herniations or of their removal. The dural sinuses
m r c not disturbed. I t was possible to remove the sagittal
snturc for most of its length, together with large portions
of both parietal bones without interfering with the sagittal
sinuses. Closure was made loy simple approximation of the
incision, and the application of 4% celloidin. Control animals
underwent incision and closure only. One hundred twenty
rats of a LongEvans strain mere used.

IIISTOLOGICAL MATERIA1,S

S o r n ia l heads f o r each age were obtained a t 1, 2, 3, 4, 7,

8, 13 and 1 G days. These were fixed at 10% formalin, and
enibedded in paraffin. Decalcification of the older specimens
 GHOTVTH O F T H E CALVABIA IN THE BAT 337

was accoinplished by the formic acid sodium citrate niethod

of Xorse ( '45). The sections were cut at 10 and 15 p i n
sagittal, horizontal and frontal planes. They were stained
routinely with hemalosylin and eosin. Occasional sections
were stained with 2 5 % aqueous toluidine blue. Some un-
decalcified sections were stained with the silver technics of
Cameron ( '30) and of McLean and Bloom ( '40). Additional
histological material froni 9 days prenatal age to 98 days of
age w t s made availahle through the courtesy of Dr. E. Apple-
baum, Department of Anatomy, Columbia TTniversity, and of
Ilr. I\-.Lefkowitz, Dental Research Laboratory, Nontefiore
H o i p i t d , S e w York City.
S O K M A I , UXO\YTII DATA

Pooled unsexed samples provided control data a t the de-

sired age levels; 161 rats of the same strain were utilized
(table 1). It has been shown that the growth of the neuro-
cranial vault of the rat, essentially complete at 34 days, shows
little di3cernible sexual differentiation at this age (RIassler
a i d Schoui-, '51). The circumnatal material represented ani-
mals removed 12-24 hours before anticipated birth. 1,itter size
was reduced to no more than 6 on the second day.

Menszwemcizts
Since these procedures involved alterations of the normal
relationships between the several cnlvarial bones, it 1vas neces-
sary to measure these bones in such a manner that the growth
of their several dimensions would be demonstrated. The
incasurements involved a modified anthropometric technic
(fig.. 2, 3).
Measurement 1 Pterion-bregma
Measurement 2 Rregma-lambda
Measurement 3 Lambda-asterion
Jlcasurement 4 Asterion-pterion
3lcasurement 5 Sasal length
Measurement 6 Xasal-lambda
Measurement 7 Projective frontal length
JIeasurement S Width of sknll (squamosal width)
338 M E L V I S L. MOSS

Alcasurenients 1, 2, 3, 4 define the two-dimeiisioiid plane

surface of the parietal hone. This area is free of iiiuscle at-
tachments. Rleasurement 3 closely approximates the temporal
crest of the adult. As the Asterion is adjacent to the most
lateral aspect of the interparietal bone, it is accurately located
TABLE 1
G1.ouG!k of the normal rat calvaria (nieasurenzents in niillinzeters)
MEASUREMENT (1) X L 4 S U R B M E N T ( 2 ) MEASUREMENT ( 3 ) MEASUREMENT ( 4 )
AQE
PTERION-BREGMA RREGMA-LAMBDA LAMRDA-ASTERION ISTERIOS-PTERION
___
days
(J-X 3.1 -1- .03 2.7 t .ll 2.2 C .12 3.5 t .03
1 4.5 t .07 3.4 F .13 3.5 F .09 4.7 t .07
2 5.3 F .ll 3.6 t .05 3.8 -t .07 L5.2 i .07
3 5.3 -c .09 4.1 t .07 4.7 F .12 6.1 F .08
4 5.4 i .07 3.8 t .08 4.5 t .09 6.2 t .12
7 5.5 i .12 4.6 C .12 5.2 rt .14 7.4 F 2 6
10 5.9 t .08 5.0 t .15 5.8 F .13 8.7 t .17
15 6.2 t .07 5.9 F .11 6.2 i .16 10.3 C .18
20 6.1 C .06 5.9 t .05 5.8 C .10 10.2 -t .15
30 6.4 i .09 6.4 t .10 6.6 C .09 11.0 & .08
34-R ' 6.1 i .05 6.1 -C .09 6.5 t .07 11.8 i .08
34-L 6.1 5z .05 6.4 F .07 11.3 -C .11

= Cireumnatal age (within 24 hours of anticipated birth).

' = Right and left respectively.
= All values are the mean values i the standard error of the mean ( n i m ) , cal-
culated for small samples.
_ _ _ -_ _~ ~

Growtk of the nownal rat calvaria

MEASUREXENT XEASUREXENT \IEASUREXENT 'rhASUREXEST

AGE (5) (6) (7) (8) SVMHPR
NASAL LENGTH UASAL LAMBDA FRONTAL L E I G T H s Q ~ ~ ~
_-
days
C-N 2.7 t .08 10.0 % .21 4.6 C .09 7.4 C .12 16
1 3.5 t .15 12.2 i .06 5.3 C .16 8.7 -t .14 11
2 4.2 C .09 13.0 C .13 5.4 i .08 9.4 t .I0 22
3 4.7 Ik .10 14.4 C .18 5.6 C .12 10.1 i . l 2 15
4 4.5 t .13 14.1 i .13 5.8 t .17 10.1 C .1G 10
7 5.3 & .12 17.7 C .23 7.7 t .09 12.2 C .36 12
10 6.3 -C- .13 18.8 Ik .23 7.4 t .15 12.7 t .I7 19
15 8.4 t .23 23.4 C .26 9.2 F .14 13.6 C .26 16
20 8.9 2 .21 23.9 & .24 9.0 -C .13 13.5 t .li 12
30 11.2 2 .24 27.3 C .12 9.8 C 21 14.0 C .09 10
34 13.5 C .11 28.2 C .23 10.6 C .13 14.3 i .08 18
___ ~ ~~~~ ~_ _ ~ _ _ _ _ _ _~-
.-- ~ ---- -- ~~ -
 G R O W T H OF T H E CALVARIA I N T H E RAT 339

even i n p e n a t a l material. Specimens measured befow the

close approximation of the individual bones, while fontanelles
were still present, necessitated a visual estimate of the inter-
section of the tangents of the dimensions involved. The 5th
measurement has been shown to be sexually dimorphic in the

I-

4-
6-
9-
II-
13-
15 -
I8 -
Fig. 2 The ralvaria of 34-day control rat. Drawn f r o m a tracing
1 Anterior nasal point 11 Junction of squania and root of
2 Nasal bone zygomatic process
3 Xasnl suture 1 2 Sagittal suture
4 Fronto-nasal suture 13 Temporal crest
5 Xasioii 14 Parietal bone
6 Frontal bone 15 Lambda
7 Metopic suture 16 Anterior lambdoid siitiii P
8 Pterion I? Aistc.rioii
9 Coronal suture 18 Iiitcrparictal bone
1 0 Bregrna

mature rat (Hatai, '07). The 6th measurement was a n overall

chord which sought to avoid the distortion which the variable
inclination of the interparietal bone would introduce into any
overall length measurement which included it. The 7th meas-
urement, the length of the metopic suture, was obtained
indirectly by subtracting the sum of measurements 2 and 5
340 RLELVIN L. MOSS

from measurement 6. Measurement 8 corresponded t o tlie

“squaniosal width’’ of Hatai (’07).
All measurements were made with small vernier calipers,
read t o the nearest 0.1mm. Those of the parietal bone were
niade on tlie right side. I n addition, bilateral measurements
wcre niade on the 34-day controls which validated the as-
sumption of cssential 1)ilateral symmetry (Howell, ’25).

Fig. 3 I )inleiisions iiic:~siiird iiidicntc.tl 011 n traciiig of skull of ront rul

rat.

1 Pterion-biegmn 5 Nasal length

11 Bregma-lambda 6 hTasal-lambda
.; Lambda-asterioii 7 Projectire frontal length
4 Asterion-pterion 8 Squamosal width of skull

Spccinicns above tlie age of 15 days were boiled, and

bleached in 3% H,O,. The change in dimensions caused by
this treatment is reportedly insignificant (Donaldson, ’19).
Specimens below this age were cleared and stained with
 G I t O W T H O F THE CALVARIA IhT THE R A T 341

alizarin red by the method of Noback and Noback ('44),

and examined with a binocular microscope.
RESULTS
E x t i r p a t i v e technics
Osseous extirpation. A portion of the right parietal bone
was extirpated. Regeneration of this area did not occur and
a thin fibrous scar tissue was found in the defect. The right
frontal bone exhibited overgrowth into the area normally
occupied by the right parietal bone. This was observed in
17 out of 18 animals operated on below 7 days of age (fig. 5).
The extent of this overgrowth could not be accounted for
by assuming it to be the lack of normal ectocranial over-
lapping of the posterior margin of the frontal bone by the
parietal bone. This was easily observed by bilateral exaniina-
tion of the endocranial surfaces. This overgrowth was a
localized phenomenon. No statistically significant alteration
of the dimensions of the neuro-cranium resulted from this
unilateral procedure. The location of the right coronal suture
was displaced posteriorly by this overgrowth. In the face of
the removal of large areas of the parietal bones bilaterally,
the overgrowth of the frontal bones became significant in
amount (fig. 6).
Identical operative procedures in 14 animals over 7 d a y
of age were not followed by overgrowth of the frontal bone
(fig. i ) .
TThen osseous regeneration occurred, no frontal bone over-
growth was observed. The normal morphology of the bones
and of the sutures was well on the way t o complete reestab-
lishnieiit at the age of sacrifice (fig. 8). This regeneration
took place by islands of bone being formed in the dura. This
result, in 4 animals, was in conformity with those obtained by
other workers with partial and total calvariectomy in juvenile
and adult forms (Heine, 1837; Troitsky, '32; Simpson et al.,
'53).
These experiments were designed t o test the concept that
the shape of the individual calvarial bones is predetermined
342 31ELVIN L. MOSS

liy the location of the sutures. The results indicate that the
butures did not primarily predetermine the morphology of the
individual bones of the skull vault of the rat during the first
post-natal week. On the contrary, the position of the sutures
seemed only to serve a s a n indication of the plane of articu-
lation between the adjacent bones. The normal location of
sutures was seemingly dependent upon the normal expansive
growth of the individual bones adjacent to these sutures.
TABlh: 2

Effect of sagittal sictiire elztiipafion 071 tlre w d f h of the t k w l l

dNU.9 mm
4-.j 29-30 Esperiniental ralne
Mean = 14.5 t .16 K = 12
34-day control m l n e
Mean = 14.3 & .08 S = 18
_ _ _ ~ ~
~- - ~ _-
._

Effect of coronal suture extirpation on the length of the skull

--~ __
.4GE AT OPERATION I’OST-OPERATIVE INTERV.Ui NASAL-LAJIRDI ( MEASUREMEST 6)

mm
30 Experimental value
Mean = 28.8 k .24 N = 12
34-day control value
Mean = 28.2 t .23 N = 18

Sutural extirputioiz. The sagittal suture was removed by

cautery or excision. The sutural tissue was removed alone
or with adjacent portions of the parietal bones. There was
no subsequent regeneration. The procedure did not cause a
significant decrease in the squamosal width of the skull (meas-
urement 8) in 1 2 animals (figs. 9, 1 0 ; table 2).
Similar procedures were applied to the coronal suture, uni-
laterally and bilaterally. I n some cases adjacent portions of
the parietal and frontal bones were removed. No regeneration
followed. These procedures did not cause a significant de-
crease in measurement 6 (Nasal-lambda) in 1 2 animals (fig.
11; table 2).
 GHO\\'TH O F THE CSLVARIA I N THE RAT 343

I'laster casts were made of some of the cases cited above

and tracings made from these casts. Comparison with tracings
of the controls proved that no deformity of the vault occurred
as a result of the sutural extirpations (fig. 4). The control
animals, with dummy incision and closure, were dimensionally
unaffected by these procedures.
These experiments were designed t o test the role of the
suture as a growth site. The results indicated that the site

J
- 32-5

conlrol
\
L
contr o I

Fig. 4 Tracings of profiles of plaster casts of aiiiuials which have undergolie

reinoral of either the sagittal suturo area or the coroiial suture area compared with
coiitrols. Casts are c u t t o approxiinate nieasurement 8, or the iuid-sagittal plane
respecti\-cly.

of growth of the sltull vault, during the period of time covered

by these experiments, cannot reside exclusively or even pri-
marily in the suture. The removal of the sutures, singly or
severally, did not cause any significant decrease in the growth
of the calvaria.
Periosfcal c r f i r p a f i o n . The external periosteum of thc
neuro-cranium was scraped and the hone burnished with
cotton. This was usually followed by burnishing with 95%
ethyl alcohol, 2% silver nitrate, and 5% phenol, applied in
various combinations. Celloidin (4% ) was applied directly
344 MELVIN L. MOSS

t o tlic bones and the edges of the skin incision were not ap-
proximated in a majority of the animals. The 39 aiiinials
utilized ranged three to 9 days of age at extirpation, and were
sacrificed 1 7 to 27 days post-operatively.
The effects of periosteal damage were evident in all cases.
The external tables were rough and pitted. In all cases there
~ v a sa displacement of sutural planes. The most coninion
finding was a n irregular anterior extension of the iiiter-
parietal bone, with consequent anterior displacement of the
anterior lambdoid suture. Other sutural areas exhibited dis-
placeineiits which varied from animal to animal. Sequestra-
tion of the sagittal sutural area occurred in the 8 aninials
operated on at three days of age in which the edges of tlie
incision were not approximated. The squamosal width of
the skull (measurement 8) was not decreased by this srqnes-
t r a t ion.
Additional cases of displacement of sutural planes conse-
quent to alteration of osseous morphology were also denion-
sti*ated. Accidental scarring of the periosteum during CRU-
tcrizatioii of sutural areas was the causative factor (figs.
12, 13).
,111 these cases of sutural displacement and osseous over-
growth had one factor in common. These was n o regeneration
of the extirpated or injured osteogenic tissues. The remaining
uninjured members of the calvarial complex seemed able to
continue their growth into areas not usually occupied by them,
with subsequent pcxssire distortion of the involved sutural
planes.
The continued growth of the calvaria following the removal
of the sutures, together with the frontal bone overgrowth
ohserved following parietal bone extirpation, tended to stress
the importance of the periosteal tissues as the active growth
site during the earliest stages and to relegate the sutures,
a s such, to a passive role during the first post-natal week.
It followed from this that the normal location of the calvarial
sutures depended on the normal growth of these periosteal
tissues, which thus determined the shape of the l m ~ c s . T,o-
caalized interfereiice of iiornial periosteal growth slioulcl then
have led to alterations of individual bone form and subse-
quent displacement of sutural planes. These results offer
evidence wliich may be interpreted a s supporting this hy-
lwthesis.

Growth of the calcaria

The growth of the skull vault of the rat was not a haphazard
process but followed a definite ontogenetic sequence. ‘Phis
is demonstrated by the data in table 1. It should be noted
that the growth of the neuro-cranium was essentially complete
a t 34 days of age, while the growth of the visceral craiiiuiii
continued long past this time. This indicated that the parietal
bones had virtually achieved their adult dimensions a t 34
days. This was also true for the posferior portion of the
frontal bones. The anterior portions of the frontal bones,
together with the other bones of the visceral complex, ex-
hibited continued growth.

I)EVELOPI\lESTAL H ISTOLOGY Ok’ CAIJVARILILEOSE

AS1) SIlTUlZE AREAS

Periods of dez;clopnzent
The histological changes occurring i n the calvarial bones
and in the sutural areas will be discussed i n detail. All cal-
varial bones pass through a similar series of developmental
pt?i*iodsfrom the onset of ossification to the achievement of
definitive form. These three periods a r e : ( a ) histodiffereii-
tiation ; ( b ) growth, which may be conveniently divided into
i i i i early and later phase; (c) definitive form. Each of these
1,criods has a distinctive histological appearance.
The bone tissue nearer the original site of ossification, at
any one instant, is more advanced in this developmental
process than the newly formed peripheral bone. Iloreover,
the various calvarial bones differ a s to the times at which
ossification begins and at which they achieve definitive form.
I n addition, within any one bone, the rate a t which various
346 MELVIN L. M O S S

portions of the bone pass through these developmental pcriods

may differ.
Periods of histodifferentiation and grozcth
(early p h a s e )
During the early phase, the greatest amount of growth
serves to extend the area of the bone to its normal shape.
The growth is very rapid in this phase with periosteal osteo-
genesis occurring on all external surfaces of the bone. E n -
dosteal reorganization results in a slight simultaneous thick-
ening of the bone which coordinates with a n extension of the
diploe.
The calrarial bones begin a s a loose mesh or network of
trabeculated bone. Ossification first occurs in a region of
looseness ” of the collagenous fibers of the neuro-cranial
( (

capsule (Graumann, ’51). I n the earliest phases of the period

of growth, the primary trabeculae, radially oriented in respect
to the ossification center, a r e interconnected by irregularly
arranged secondary trabeculae. Enclosed within this o s e o u s
network a r e non-osseous areas. The free trabeculated cdgcs
of the bones, consisting of horizontal, unilainiiiar spicules,
end in a dense connective tissue which is the residue of the
original membranous neuro-cranial capsule (figs. 14, 15).
The extent to which this capsule is replaced by bone in-
creases centrifugally f roin the centers of ossification. The
region between these expanding centers is the presumptive
suture. As the period of growth progresses, the bone as a
whole passes from a loosely trabeculated open spongy net-
work, through a solid plate stage, to a more highly organized
tissue exhibiting inner and outer tables of compact bone,
with an intervening diploe of spongy bone. The bone tissue
changes by R process of internal reorganization and reorien-
tation of the osteones, from a reticular, non-laminated struc-
ture, to one which is laminar in character. I n areas where
there is no diploe, vascular channels a r e seen within this
comparatively dense bone. The homologous development of
the human calvaria is reported by Xoback ( ’43).
 GROWTH O F THE CALVARIA IN THE RAT 347

The sutural areas are in the stage of the presumptive suture

during the periods of histodifferentiation and of growth. Con-
comitant with the osseous changes, the sutural tissues undergo
certain definite transformations. The presumptive sutural
tissue becomes increasingly cellular as its extent is diminished
by the approaching bones. Packing and crowding of these
cells is especially evident where the sutural tissues are com-
pressed between the reciprocally bevelled edges of squamous
suture, such as the coronal. There is no differentiation of the
presumptive suture, during the period of growth into the
three-layered structure which will be described later as char-
acteristic of the definitive suture.
The presumptive suture in an area which allows for con-
tinued soft tissue growth, and for compensatory adjustments
between bones during the periods of differentiation and
growth. It also yields certain mechanical advantages to the
skull (Mijsberg, '32; Giblin and Alley, '44).
There is evidence of peripheral osteogenesis at the sutural
area. By this means the bones continue to expand in surface
area. The most peripheral osteoblasts appear to be con-
tinuous with the periosteal layers surrounding the more cen-
trally located portions of the bone. These layers are simul-
taneously osteogenic. They do not connect with similar layers
about adjacent bones across the suture.
The various neuro-cranial sutural areas of the rat complete
this early phase of the period of growth at about the same
age. The coronal suture passes into the latter phase of the
period of growth at approximately the 7th day, as do the
metopic and sagittal sutures. The fronto-nasal suture has
passed through this phase before birth.

Period of growth ( l a t e p h a s e )
This late phase is characterized by the limitation of the
extent of the presumptive suture. This non-osseous area is
now relatively much narrower than in the previous phase,
except at the regions of the fontanelles. Osteogenesis con-
tinues to be active on all surfaces of the bones.
348 M E L V I F L. MOSS

As this phase continues, relatively greater emphasis is

given to increasing the thickness of the bone, and to its in-
ternal reorganization. Growth at the sutural areas continues
to extend the surface area of the bone but to a lesser degree
than in the early phase. At the completion of this phase,
the fontanelles are closed and the bone has assumed its
definitive form. Throughout this late phase of growth, greater
areas of the bones become centrifugally reorganized. Finally,
the bone at the periphery assumes a histological appearance
similar to that of the more centrally located portions.
In this reorganizational process, the peripheral bone at
the sutural area shows a transitional structure. At the pe-
riphery, the unilaminar spicules disappear and are replaced
by several layers of irregularly disposed trabeculae (fig. 16).
These horizontally oriented trabeculae extend their several
free edges into the increasingly cellular presumptive sutural
tissue. The development and peripheral extension of the
diploe is a simultaneously continuous process. As the pe-
riphery of the bone expands, the diploe extends into this
newly formed osseous tissue, always a little behind the ex-
pansion of the bone. This extension of the diploe is neces-
sarily accompanied by periosteal accretion on both the inner
and outer compact layers of the bone, and by the resorptive
processes occurring within the bone.
While the periphery of the bone is in a unilaminar state,
the diploe is a closed cavity. With the onset of the thickening
multilaminar transitional stage, the diploe comes into direct
continuity with the soft tissues of the sutural area (fig. 17).
The transition between the late phase of the period of
growth and the period of definitive form occurs slowly. The
histological picture of the sutural areas changes gradually.
The neuro-cranial sutures of the rat exhibit the histological
picture of the period of definitive form during the third week.
When the posterior portion of the frontal bone, as defined
by the coronal suture, has entered this stage of development,
the anterior portion of this bone, as defined by the naso-frontal
 GROWTH O F THE CALVARIA IN THE RAT 349

suture, is still in the late phase of the period of growth and

will remain in this period until well past the third month.

Period of definitive f o r m

A bone continues to grow after it has achieved its definitive

form. Osteogenic activity is noted at limited areas of the
inner and outer tables. Internal reorganization of the bone
continues. Laminar bone replaces the remaining trabecular
structures. This is an expression of the greatly decreased
rate of growth (Amprino, ’47).
A continuous osteogenesis occurs at the sutural areas. The
individual bones, which have already attained definitive form,
continue to grow slightly t o their final adult size. This growth
is mutually adjustive between adjacent bones and the final
position of the definitive suture is thereby attained. The
transitional structure of the peripheral bone during the pre-
ceding phase of growth is now replaced by direct osseous
continuity of the inner and outer tables at the sutural area.
The periphery of the bone, in effect, becomes “sealed off.’’
The diploe again becomes a closed cavity, no longer in open
continuity with the connective tissues of the sutural area
(fig. 18).
I n time, the sutural tissue passes insensibly into the three-
layered state described by Weinmann and Sicher ( ’47), with
a middle cellular layer surrounded by two fibrous layers. It
should be emphasized that this histological picture is charac-
teristic of only a relatively old suture. This is the stage of
the definitive suture; that is, it appears only after the bones
adjoining the suture have achieved definitive form. The de-
finitive suture, which replaced the earlier structure, now serves
as the chief site of further small adjustive growth processes.
It continues t o furnish mechanical advantage to the skull
(Wetzel, ’24; Cobb, ’40). I n turn, this picture of the suture
gives way t o that later appearance which is characteristic
of the final stage of development of the sutural tissue. Ex-
cepting ossification, this is the transformation of the three-
350 M E L V I N L. n f O S S

layered soft tissue structure into a tissue which is almost

completely fibrous (fig. 19). Beriistein ( ’33) and Erdheim
( ’ 3 8 ) give comprehensive reviews of these developmental
periods f o r human material.

G r o ss o h s e ri (iti ons
‘

Examination of a series of cleared, alizarin-stained normal

speciniens, with a biiiocular microscope, gave a vivid picture
of these developmental processes. The distinction between
the open traheculai meshwork of the earlier phases stood in
marked contrast to the smooth, deeply staining edges of the
older phases. The chroiiology of sutural area developmen t
was confirmed by this method. It was also noted that the
maturation of the sagittal suture area began posteriorly and
proceeded towa1.d the bregma, while the coronal sutural area
proceeded in a medial direction toward the same point.

DISCESSIOK

The observed overgrowth of the frontal bone into an area

formerly occupied by a n extirpated parietal bone, together
with the shifting of sutural location after periosteal injury,
casts doubt on the concept that “the sutures a r e topographi-
cally determined elements of the head, they form boundaries,
beyond which the growth of the bones cannot extend” (Troit-
sky, ’ 3 2 ) . This overgrowth and sutural shifting indicate that
the location of the sutures cannot primarily predetermine this
morphology of the calvarial bones. Rather, the sutures appear
to be lines of demarcation between unfused osseous tissues,
which arise from separate ossification centers (Hasselwander,
’38). This concept appears to be borne out by the frequent
findings of supernumerary sutures in primates and man.
Some of these sutures can only serve to indicate ununited
portions which arise from separate ossification centers and
normally fuse. F o r example, the metopic suture may persist
in such a situation. Others of these supernumerary sutures
separate osseous tissues which arise from supernumerary
 GRO\VT€I O F T H E CALVARIA I N THE R S T 351

ossification centers (Augier, '31; Peters, '32). That a suture

exists only so long a s fusion between bone arising from sepa-
rate ossification centers has not occurred is shown i n the
case of the human incisive suture (Noback and ~ I O S '53).
S,
Iletermipzation. of sutural position
No conflict exists between the findings of Troitsky ('32)
that the calvarial bones would not cross sutural planes, and
the frontal bone overgrowth and sutural displacement re-
ported in this paper. Troitsky, unfortunately, extrapolated
his interpretation of the results of extirpativc procedures on
juvenile forms to the earlier periods of growth. The bones
of these older animals have already passed through the early
phase of the period of growth. Troitsky explains the lack of
overgrowth as being due to the discontinuity of osteogenic
layers of adjacent bones across the sutural areas at the age
of extirpation. This cannot be the reason, a s has been shown,
for the lack of continuity existing i n the youngest stages
observed.
Osseous overgrowth following extirpation of a n adjacent
bone is, apparently, not a function of the histological develop-
ment of the soft tissues of the suture. It depends on the
period of development of the peripheral borders of the ad-
jacent bone at the sutural areas.
The observed frontal bone overgrowth did not occur after
7 days of age. It seems likely that this is related to the histo-
logical alteration of the periphery of the frontal and parietal
bones at the coronal sutural area. A t this age, these portions
of the bones enter into the latter phase of the period of growth.
Their peripheral borders assume the multilaminated, open,
transitional form noted above. When the bones pass into
the latter phase of the period of growth, the position of the
suture becomes determined in relation to the bone. There-
after, the suture will maintain its position in the face of
O S S ~ O U Sextirpation.
Periosteal extirpation, on the other hand, is followed by
sutural displacement even if this operative procedure is ap-
352 MELVIN L. MOSS

plied to animals older than 7 days of age. The conditions of

this series of experiments, however, differ from those of
osseous extirpation. The latter animals have all of their
remaining periosteal tissues intact. This allows for the un-
interrupted sequence of developmental processes which are
a function of these periosteal tissues.
I t would appear that both of the seemingly opposed con-
tentions concerning the relationship of the location of the
suture to the form of the calvarial bones a r e correct. The
location of the suture is primarily determined by the growth
of the adjacent bones. The suture indicates a plane of articu-
lation between them. The growth in surface area of these
bones is determined, in part, by the fibrous orientation of
the neuro-cranial capsule (Thoma, ’11; Kakott, ’33). To this
vxtent, the location of the presumptive suture is “topo-
graphically determined.” This determination of position is
altered in the face of timely extirpation of adjacent bones
o r of periosteal tissues.
It is not that the suture forms “ a boundary beyond which
the bones cannot extend,’’ but rather that the period of de-
velopment of the osseous tissue itself at the time of extirpa-
tion determines whether this overgrowth will occur.

M o d e of growth
The results of the sutural extirpation experiments, together
with those of periosteal extirpation, indicate that the suture
is not the primary, active site of growth of the calvaria.
Specifically, the growth of the rat neuro-cranium is not ac-
complished by means of a n interstitial expansive force origi-
nating within the soft tissues of the suture. The periosteal
osteogenic tissues, ectocranial a s well as endocranial, appear
to be the primary growth sites.
Utilizing this hypothesis, together with the data presented
on the developmental histolo,gy of the calvaria, it is possible
to present a conception of the growth of the skull vault which
will more adequately account for all of the available data.
 GROWTH O F THE CALVARIA I N THE RAT 353

In so doing, it is shown that the views of the contending

schools of thought, concerning the role of the suture in the
growth of the vault, are not antagonistic but rather comple-
mentary.
The growth of the calvarial bones is primarily a function
of the periosteal tissues surrounding all surfaces of the bones.
The sutural area is but one site of periosteal osteogenesis
during the period of growth of the skull vault. Osteogenesis
occurs on all the surfaces of the rat calvaria under 60 days of
age (Xassler and Schour, ,Ejl). The centrifugal expansion of
the skull vault is a response to the expansion of the brain
(Hauschild, ’31;Mair, ’26; Sitsen, ’33). I n this sense, the
bones “float ” outward, being passively carried within the
neuro-cranial capsule, which is expanding to accommodate the
increasing volume of the brain. The bones constantly increase
their surface area by peripheral extension of their periosteal
layers into the presumptive sutural areas.
Calvarial bone formation, at the sutural areas, observed
by an alizarin staining technic or by a marker implant technic
(Giblin and Alley, ’42), during the period of growth, will
appear to show osteogenesis within the suture. This illusion,
of course, is due to the fact that almost all of the new bone
tissue has been added to the borders of the older bone tissue
at the sutural area as the bone is increasing in surface area.
This conclusion is in harmony with the views of Thoma ( ’13),
Sicher ( ’ 2 1 ) and Bernstein (’33). The extents of the pre-
sumptive sutural areas are maintained relatively constant
during this process. If the peripheral accretion of bone is
not coordinated with the internal forces of expansion, ex-
cessively wide sutural areas will result. This is found to be
the case in hydrocephalus.
Evidence of endocranial apposition, in the early stages of
development of the calvarial bones, is only a n indication that
these bones are increasing in thickness concurrently with the
expansion of the diploe. When the bones have attained defini-
tive form, it is not surprising that the only sites of osteo-
genesis would be the areas of muscle attachment on the ecto-
334 MELVIN L. MOSS

cranial surface and at certain definite sutural areas. The

former is a means of adapting to increasing muscle mass,
while the latter provides f o r a relatively minor adjustment
of sutural architecture, which may yield additional mechanical
advantage.
The point to be stressed is, perhaps, not that the periosteal
tissues arc the sites of calvarial growth during the period of
growth, but rather that there is no suture (i.e., definitive
suture) at this stage which could serve as a site of growth.
Indeed, the soft tissues of the sutural area are in the stage
of the presumptive suture throughout this period when the
greatest amount of calvarial expansion is occurring. The
sutural areas do not, then, possess the histological structure
which has been postulated (Weinmann and Sicher, '47) as
necessary for the existence of an expansive force in this
tissue.
S o conflict of theories concerning the sites of growth of
the skull vault exists if one is careful to distinguish: ( a ) the
site of growth studied, together with (b) the stage of develop-
ment of the bones and soft sutural tissues a t the area of
study, for the particular animal form under investigation.
When these two factors are considered, the experimental
data in the literature are capable of resolution. I n this con-
nection, it is necessary to evaluate the seemingly conflicting
views of Brash ( '34) and of Massler and Schour ( '51).
Using madder-fed juvenile and young adult pigs, Brash
concludes that the growth of the skull vault is essentially a
process of ectocranial accretion and endocranial resorption,
with the suture playing only a minor adjustive role. It is
clear, however, from the illustrations in Brash's work, that
the calvarial bones of his animals have already passed through
the period of growth. They have already achieved most of
their thickness and are engaged in the process of altering the
curvature of the calvaria. The bones have achieved definitive
form. No further increase in surface area is to be expected.
The sutural areas are in the stage of the definitive suture.
 GROWTH O F T H E CALVABIA IN THE R I T 355

On the other hand, Xassler and Schour feel they have dis-
proved Brash’s concepts in two ways. First, by their finding
of osteogenesis on all surfaces of the rat calvarial bones below
60 days of age; a n d second, by the undoubted accretion of
bone at the periphery of the sutural areas. These younger
forms, however, have been studied while the bones were still
i n the period of growth, and undergoing a n increase in sur-
face area a s well a s a n increase in thickness. The sutural
areas a r e in the stage of the presumptive suture in these
younger forms. These sutures a r e only gradually transformed
into the stage of the definitive suture.
However, if a comparison is made between Brash’s find-
ings and those of his critics on rats past 60 days of age, the
results a r e identical. A t this age, the rat and the pig show
osteogenesis on only certain ectocranial areas and in certain
definitive sutures. The calvaria of the rat, however, docs not
undergo the alteration of calvarial curvature to the extent
that the pig does.
It is now clear that in reality both workers are reporting
complementary studies of different stages of one unified
process.
coNcLu8IoiYs
The growth of the iimro-cranium of the rat is essentially
complete at 34 days, while the growth of the visceral cranium
continues well past this age. The two poi*tions of the calvaria
develop at different r a tes. The individual calvarial bones
pass through a series of characteristic histological stages
during this developmental process. Simultaneously, the con-
tiguous soft tissue areas a r e transformed from the stage of
the presumptive sutni-e to that of the definitive suture.
The influence of these sutural tissues on the growth and
consequent shape of the rat calvaria a r e investigated by a
variety of extirpative technics. The normal calvarial mor-
phology depends on the osteogenic activity of all the perios-
teal tissues. Thc shape of the calvarial bones is not prede-
termined by the location of the sutures. It is possible to
produce overgrowth of calvarial bones by many methods
336 MISLT’IS L. MOSS

\\.it11 coilsequelit displacement of sutural positioii. This phe-

nomeiioii appears to depend on the period of development of
the osseous tissue. Calvarial sutures mark the plane of articu-
lation htweeri adjacent hones. The location of the sutures
is detcrmined by the relative growtli of the adjaceiit Iiones.
The neuro-cranial suturvs a r e not the chief sites of gi-owtli.
The vsistencc of a n expansive force within the sutures during
the period of greatest growth is not substantiated. Extirpa-
tion of the sutures, siiigly or seveidly, is not followed by any
decrease iii either width OY length of the calvaria.
A11 interpretation of calvarial growth is presented v7ihich
harmonizes the conflictiiig vicws on the iiature of the suture
and its role a s a growth site. T’hen allo\vance is niadr foi.
the pci.iod of devclopmeiit of the site of gro~7thof the par-
ticulwt. aiiinial under investigation, all of the previous coil-
ceptioiis a r e shown to be complementary.

L I T ER,.kTCRI.; (!I TI.: I)

ANPRISO, R. 1 9 4 i La structure tlu tissu osscux eiivis:igee de differciiees dmis
1:1 ritesse de 1 ’;iccroisscment. Arch. R i d . P:iris, 5 8 : 315-330.
A r m R i ? , If. 1931 111: Poirier, P., and A. Cliaqiy, Trait? 1)’An:itoniie 1Tiiin:iiiic.
Paris, 3f:issoii et Cie.
EIS, S. A. 1933 i?l)er tlen iioriiialrii Iiistologisclien Auflmu drr Srlildel-
d:iclis. %it. f . :inat. u. TI:iitn.ichlungsgesch., 701 : G2.5-Gi8.
P,R.%sIf, J . (1. 1934 Some p I T J h h I S 011 tlic growth and dcve1opment;il iiier1i;iiiic.s
of h i i c . E3diiil.i. Med. J., 4 7 ; 305-319, 3 6 3 - 3 8 i .
CAIIF:ROX, G. R. 1930 Tlir staiiiiiig of calcium. J . Patli. Bact., 3 3 : 929-955.
COBB, W. M. 1 9 4 0 Tlics rI:i~io-f;ici;iI ~niioiiiii iiiaii. A m J . Pliys. Aiitlirop., ,26:
87-11 1.
DON-HJDSON, IT. 11. 1919 Gromtli of tlir skcleton of tlic albino rat. Ain. .J. Annt.,
2 G : 237-314.
1+i1~1mrir, J. 1938 l k r Geliir~isclliitlel iii seiiier Rezicliung ziiiii Geliirn iiiitcr
iioriiinlen und pathologislieii riiistiiiideii. Viwliows Arrlii\-. f. Patli.
An:it., 302 : ili3-818.
GIIUJS, S.,A X I I A . ALLEY 1942 A nictliod f o r 1ne;isuring lioiie growth i n tlic
skiill. Ailat. Ere., 8.7: 381-387.
-___ 1944 Studies in skiill growth. Co:oii:il suture fixation. Anat. Rec.,
8 8 ; 143-153.
, W. 1951 T O J J O ~ C Ider I C SEintlcge\~el~eskiioclieii.
~ Uiit,ersiicliungen
a n Bch~dclknocheii niriiscliliclit~n Eiiil)i,yoiic,ii. &it. f . annt. 11. l3ntrnit.h-
llungSgescll., I16 : 1-1:1.
GLTDES, B. voiv 1874 Kxperinieiit:il T7iitcrsiicliungeii Ubcr des Scliadcl\~~iclistiiur.
Municli, cited in Troitsky, 1932.
~I.\SSELIV.\SDER, A . 1938 I n : H:mdl~ucllder hnatoniie des Kindes. Ed. .T. Berg-
nian, Munich, ,?: 403-489.
FhT.41, S. 1907 Studies 011 tlic v:iri:ition :rnd correl;rtion of skull ineasurenwnts
in )jot11 sexes of mature albiiio rats. Am. J. Anat., 7 : 423-441.
H I L D , 31. W. 1921 Histologisclie TJntersncl~ungen iiher norinale mid a l j -
norine Synostose der Hil.iiscliKdelii:iIite. Vcrlranill. (1. Anat. Gesellscll.,
85: 85-93.
H 1 < 1 S b : , R. 1837 In: Bernlinrcl IIctines Versuc.lie nkwr I~iioclii~iiregcn(~~:ition. Ed.
Redenz, E., and H. K:iltclr (192G), Berlin, .J. Springer.
HOW:LL,A. R. 1925 Asyinmrtry in the skull of nianininls. Proe. U. S. S:it. >riis.,
G? : ZTo. 27, 1-18.
K O K O T T , IT-. 1933 Uber deli B:in1)1:1n drs fotalen HiriiscllZdels. Gegrnlxiuers
Morpliol. Jahrb., 7 q : 341-361.
hf.lIR, 13. 1926 Untersucliongen iiher die Stroktur drr Scliiidelknoclirii. Zeit. f .
niikroskop. Anat. Forscliuilg., ;i: 625-667.
Jl.\SSI.EK, JI., ASD I. SCHOUR. 1951 The growth pattern of t h e cranial w n l t iu
the albino r a t a s nie:is11rd l ) v~ i t a l staining with alizarin red 'IS."
-Inat. Rce., 130: 83-101.
3r('IAI~:-\~. F. C"., .\ND r\. KLooJr 1940 Calcification and ossific:ition.. (":ilcification
in norrnal growing hone. Aiiirt. Rcc., 7 8 : 333-359.
hfI.JSBER(;, W. .\. 1932 Die Fnnetion der Kiihte a m waclisriiden Scliiidcl. Zeit.
f . irorpil. 11. ~ ~ ~ t i l r om:
p . ,~ 3 ~ 5 5 1 .
~ I O X S.I. X , 1945 Forniic aciil-sodiuln citrntc decalcification and butyl alcohol
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dcrcloInnent of the Iiunl:in embr?onic, fetnl und circumn:ital skeleton.
Anat. Ree., 8 7 : 29-57.
X Q B . W I i . C. R., .\SD hi. L. NOSS 1953 Topology of t l i c Iiiiinnn p ~ - n i ~ i x i l l a ~ ~
hone. Am. J . Pliys. Antlimp., 7 7 : 181-1 8X.
170R\(K, c'. R., AND E. NOBA('K 1944 I)emonstratinq tht, osscons skeleton of
Iinman embryos :rnd fetuses. Stain Teclr., I!) : 5 - 5 4 .
RS, H. K. 1932 t l ~ K5.lit-Anoin(~lirn
r und T:iri:rt,ion an Priinatrn Cranium.
Zeit. f . Norph. ti. Anthrop., S O : 317-3T2.
RICHER, L. 1921 Zur Kciintnis des \Trcicli und IJiiekensrlliidrls. F w n k f . Zeit.
f . Path., ,%: 497-525.
SrarPscs, M. E., D. C. VAN I)YKE, C. W. A s r J r ~ c ,A N D H. M. E v a i ~ s 1953 Re-
generation of the rat calvarium i n young norm:il a n d grontli hormone
treated Ir~~opliysectoniizecl rats. L\nat. Rrc., 1 7 5 : 615-626.
-, E. 1933 Zur Entwicklung der Xiilltc dcr ScliadeldZclirs. Zeit. f .
Annt. u. Ent~iclilungsg.escli.,101 : 121-153.
T'iIoir.*, K. 1911 TTiitersuc~Iiuiigeni i l das ~ Scliadel~~aelistiim iind seiner Stolunq.
(1) Die Spannuiig der Sch>idelw:ind. Virchows Areliiv., .?OS: 201-2il.
.-__ 1913 Ibid. ( 2 ) Das fot:ile W:iclistnm. Thid., .?1?: 1-67.
TRoIi%i.;x-, W. 1.932 Zur Frage der Forml)ildungen dcs Scll6deldncli:~s. Zeit. f .
3Iorpli. 11. Anthrop., 90 : J04-332.
358 JIELVIN L. MOSS

WEINMAXN, J. P., AND €1. SICHEH1947 Bone and Bones. St. Louis, c. V. JIoshy.
WETZEL,G. 1924 Studien zur Schadelststik: Funktionelle Rtruktur der SElite.
Grad. der Sicherheit Gengeniiber Beanspruchung. ~ ~ e r l i n u d (1.
l. h i a t .
Gesellsch., 33-4i. .Jena, C. Fischer.

PLATE I
ESPLANATIOX OF F I G C X E S

Graphite has bee11 1)urnished into tlie sutures to aid iii their il1ustr:itioii

S o t e overgrowth of frontal boiie into area of extirpated parietal bonp with

consequent displ:icenient of tht, coroiial suture. Animal operated on a t ti days
and seerificed a t ti8 days.
Bilateral renioval of 1:irge portions of parietal bones. S o t e kirk of s:rgittul
suture area. hlensuronient 7 (projective frontal length) is significantly greater
than control v:ilnes. Also note aiiterior displacement of right anterior Iambdoid
suture. Lack of sagittal suture did not decrease squamosal width of the skull
(measurement 8). Animal operated on a t 4 days aiid s:icrifieed a t 34 days.
S o t e hick of front:il b o ~ wovergrowth i n rat operated on a t 1 0 (lays of agc’
and sacrificed a t i 2 days.
Regener;ition within area of cxtirlxition. Xote is1:intls of bone a t tlie coronal
sutural area. Anini:iI operated on a t 6 days and s:rcrificed :it 35 days. Orer-
growth of the front:tl bone, did not occur.

9-70 Cauterizatioii of the sagitt:il aiid metopic siitrir:rl areas a t 5 da)-s of :igc
and sacrificed :it 31 (lays. All of tlie folloniiiy rats were opewted on aud
sacrificed a t the same ayes. Squ:tniosal width not decreased.

11 Eilateral cautery of the coronal sutinxl :irca. Aiitelo-li(isttc.1ior dinicnsions

:ire significantly affected.

12 Chuterp of the riglit cornnal sutural are:i with accidental scarring of the
surrounding priostenni. Note shift of right aiiterior Iniiil~doid suture :in-
teriorly.

13 Cautery of the left coronal sutural area with aecideiital scarring of the sur-
rounding periosteuni. Xote shift of the sagittal sutiirc toivartls tlir left, a t
the bregma.
359
 ESPLlNATION O F FIGrRES

,\I1 ~ilioto~iiic.rogr:iplis
are oricntcd with the ectocraninl surf;icr uppermost

14 Sagittal sotur:il area of the newborn rat. Kote tlica unil:iminar state of tlic
periphery of the hones. This and the following figure arc c1i:ir:ictcristic of
the early p h s c of tlic pciikd of growth. 2% silver nitr:ite.
15 Coroii:il sutur:rl area of tlie newliorii nit. 2% silver nitr:itc.

Ifi Sagittal sutural area of tlie 8-d:iy rat. Sotcb tlic inrilti1ainin:ir ;iljpwr:iItcc of
the peri1jliery of the bone. This is tlic stage of the trnnsition:il structure
wliicli is ch:iracteristic of the later 1iIi:ise of the lieriod of growtli.

17 Cornxi1 suture of the 8-day nit. S o t e t1i:it in this tr:insitioii:il structiirc the
diploc is in dirrct cont:ict wit11 tlic sutural tissues.

18 Coronal sutural area of the 1G-tl:iy rat. Kotc tlie direct osseous continuity
of the t:iblcs of Iioiic a t tlic pcripliery. Tlic transitional structurc has dis-
:ippcxred. Tlic rliplot~is iio longer in direct coiit:ict with the sutural tissues.
n ratc of growtli is rapidly decrcwsiiig.
This is n cli:ir:icteristic picture ~ d i c ~the
19 (‘oron:il sutiirr of the 98-day rat. This is :I definitive suture in the period of
definitive forni.
301