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Paleoneurology is an important research field for studies of human evolution. Variations in the size and shape of the endocranium are a useful means of distinguishing between different hominin species, while brain asymmetry is related to behaviour and cognitive capacities. The evolution of the hominin brain is well documented and substantial literature has been produced on this topic, mostly from studies of endocranial casts, or endocasts. However, we have only little information about variations in endocranial form, size and shape in fossil anatomically modern Homo sapiens (AMH) and about the evolution of the brain since the emergence of our species. One good illustration of this limited knowledge is that one of the first fossil H. sapiens discovered, in 1868, that is also one of the oldest well-preserved European specimen has never been studied in what concerns its endocranial morphology. The first aim of this study was to propose a detailed description of the endocranial anatomy of Cro-Magnon 1, using imaging methodologies, including an original methodology to quantify endocranial asymmetries. The second aim was to compare samples of the fossil and extant AMH in order to document differences in the form, size and shape of the endocasts. A decrease in absolute endocranial size since the Upper Palaeolithic was noticeable. Although both extant and older endocrania have the same anatomical layout, we nonetheless found non-allometric differences in the relative size and organization of different parts of the brain. These document previously unknown intraspecific anatomical variations in the H. sapiens brain, demonstrating its plasticity, with some areas (frontal and occipital lobes) having been more subject to variation than others (parietal, temporal or cerebellar lobes). That may be due to constraints to maintain an optimal performance while reducing in size and changing in shape during our recent evolution.
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ARTICLE / ARTICLE
First description of the Cro-Magnon 1 endocast and study of brain
variation and evolution in anatomically modern Homo sapiens
Première description de lendocrâne de Cro-Magnon 1 et étude de la variation
et de lévolution du cerveau chez les Hommes anatomiquement modernes
A. Balzeau · D. Grimaud-Hervé · F. Détroit · R.L. Holloway · B. Combès · S. Prima
Received: 23 May 2012, Accepted: 10 September 2012
© Société danthropologie de Paris et Springer-Verlag France 2012
Abstract Paleoneurology is an important research field for
studies of human evolution. Variations in the size and
shape of the endocranium are a useful means of distin-
guishing between different hominin species, while brain
asymmetry is related to behaviour and cognitive capaci-
ties. The evolution of the hominin brain is well documen-
ted and substantial literature has been produced on this
topic, mostly from studies of endocranial casts, or endo-
casts. However, we have only little information about var-
iations in endocranial form, size and shape in fossil
anatomically modern Homo sapiens (AMH) and about
the evolution of the brain since the emergence of our spe-
cies. One good illustration of this limited knowledge is
that one of the first fossil H. sapiens discovered, in
1868, that is also one of the oldest well-preserved Euro-
pean specimen has never been studied in what concerns its
endocranial morphology. The first aim of this study was to
propose a detailed description of the endocranial anatomy
of Cro-Magnon 1, using imaging methodologies, includ-
ing an original methodology to quantify endocranial
asymmetries. The second aim was to compare samples of
the fossil and extant AMH in order to document differ-
ences in the form, size and shape of the endocasts. A
decrease in absolute endocranial size since the Upper
Palaeolithic was noticeable. Although both extant and
older endocrania have the same anatomical layout, we
nonetheless found non-allometric differences in the rela-
tive size and organization of different parts of the brain.
These document previously unknown intraspecific ana-
tomical variations in the H. sapiens brain, demonstrating
its plasticity, with some areas (frontal and occipital lobes)
having been more subject to variation than others (parie-
tal, temporal or cerebellar lobes). That may be due to
constraints to maintain an optimal performance while
reducing in size and changing in shape during our recent
evolution.
Keywords Endocasts · Homo sapiens · Cro-Magnon ·
Brain evolution · Paleoneurology · Asymmetry
Résumé La paléoneurologie est un champ de recherche
important dans le cadre des études sur lévolution humaine.
Les variations de taille et de forme de lendocrâne sont
en effet utiles pour différencier les différentes espèces
dhomininés, alors que les asymétries cérébrales sont
reliées au comportement et aux capacités cognitives. Pour-
tant, notre connaissance de lévolution et de la variation du
cerveau dHomo sapiens, depuis lapparition de notre
espèce, est très lacunaire. Dans un premier temps, nous
détaillons lanatomie et les asymétries (en proposant une
méthode innovante de quantification de ces dernières) de
lendocrâne de Cro-Magnon 1, un des représentants eur-
opéens les mieux conservés et les plus anciens des
Hommes anatomiquement modernes, qui navait encore
pu être analysé. Puis, une étude comparative entre un
échantillon de spécimens fossiles et actuels dHomo sapi-
ens est effectuée. Bien quun substrat anatomique commun
soit présent, certaines différences de taille et dorganisation
A. Balzeau (*) · D. Grimaud-Hervé · F. Détroit
Département de préhistoire du Muséum national dHistoire
naturelle, équipe de paléontologie humaine,
UMR 7194 du CNRS, Paris, France
e-mail : abalzeau@mnhn.fr
R.L. Holloway
Department of Anthropology, Columbia University,
New York NY 10027, USA
B. Combès · S. Prima
Inserm, U746, F-35042 Rennes, France
INRIA, VisAGeS Project-Team, F-35042 Rennes, France
University of Rennes-I, CNRS, UMR 6074, IRISA,
F-35042 Rennes, France
Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
DOI 10.1007/s13219-012-0069-z
ont été observées entre ces deux échantillons. Ces résultats
illustrent la plasticité du cerveau au sein de notre espèce et
documentent une variabilité anatomique encore inconnue.
Mots clés Endocrânes · Homo sapiens · Cro-Magnon ·
Évolution cérébrale · Paléoneurologie · Asymétrie
Introduction
Paleoneurology is a major field of research in paleoanthro-
pology, which has produced abundant literature document-
ing the evolution of the hominin brain [13]. However,
although we have a fairly good overview of the evolution
and variation of endocranial anatomy in the different homi-
nin species during the 7 Ma of human history, and more
particularly in the last 3 Ma, our knowledge and understand-
ing of variations and modifications of the brain in anatomi-
cally modern Homo sapiens (AMH) in the last 200,000 years
is very patchy. This is partly due to the limited material avail-
able and the small amount of published data about endocasts
of fossil H. sapiens.
In 1868, five human skeletons, corresponding to four
adults and a child, were exhumed in the Cro-Magnon rock
shelter located in Les Eyzies-de-Tayac, near the town of Sar-
lat in Dordogne, France [47]. This discovery was of para-
mount importance at the time: while the antiquity of man
was definitely accepted as a fact, these remains were
among the first fossil specimens attributed to H. sapiens.
Anthropologists concluded that they represented a Cro-
Magnon race[810]. This typology is not in use anymore,
but the term Cro-Magnonis still used in popular science
literature, and sometimes by scientists, as a synonym for
prehistoric man and/or to refer to anatomically modern fossil
H. sapiens found in Europe. Since their discovery, several
detailed anatomical studies have been performed on the Cro-
Magnon fossils [5,6,1012]. The first individual (subject
No. 1), initially referred to as the old man, has also
been the focus of many palaeopathology studies because of
intriguing macroscopic bone lesions [5,6,10,11,1315]. The
remains unearthed in the Cro-Magnon site were originally
attributed to the Aurignacian period but this question has
been much debated. Since then, a date of 30,000 BP was
first proposed by comparison with the
14
C dates obtained
for the Aurignacian sequence from the Abri Pataud in Dor-
dogne [16]. However, dating of a shell ornament recently
found in association with the human remains suggests an
age not earlier than 28,000 BP. The burial could therefore
be attributed to the Gravettian period [17]. The very good
state of preservation of the Cro-Magnon 1 skull made it
impossible to reach its internal features, but a detailed
study of data obtained from imaging methodologies (CT
scans) gave us access to a whole series of internal anatomical
structures for this specimen, such as pneumatisation of the
facial and temporal bone, cranial vault thickness and struc-
tural bone composition, allowing us to supplement previous
anatomical descriptions of this specimen (Fig. 1).
We have only little information about variations in endo-
cranial anatomy, size and shape in fossil AMH, and the evo-
lution of the H. sapiens brain since the emergence of our
species is poorly documented. A gradual and relatively
small decrease in absolute endocranial size since the Upper
Palaeolithic was previously reported (e.g., [18]). It has been
proposed that this trend could be explained as an allometric
decrease based on a loss of bony/muscular robusticity, with-
out any significant behavioural association[2,19], or could
be correlated with a reduction in body size [18]. However,
these interpretations lack sufficient demonstration because
of the limited data available. More importantly, no informa-
tion is currently available about a possible correlation
between variations in the shape and structure of the brain
and this decrease in absolute size. This is an important limi-
tation to recent efforts drawing on developments in brain
mapping and computational anatomy in living humans that
aim to analyse brain structure and function in order to docu-
ment variations in the H. sapiens brain.
Given this context, this study has two major objectives.
The first is to describe the internal cranial anatomy of Cro-
Magnon 1, and particularly its endocast, accessed thanks to
imaging methodologies. Because of the excellent state of
preservation and completeness of the specimen, its endocra-
nial surface has never been casted, and therefore never been
studied. Our second aim is to document the differences in
form, size and shape of the endocast between extant and
anatomically modern fossil H. sapiens, using all the fossil
specimens available and a very broad sample of extant
humans.
Material
In Africa, the oldest attested AMH are Omo 1 [20] and Herto
Bouri [21], aged 195,000 and 154,000 years respectively.
Omo 1 is rather incomplete and Herto Bouri has not been
exhaustively studied as yet and its endocast has not been
described. Then there is a gap in fairly complete African
specimens [22] until the Epipaleolithic populations from
Afalou-Bou-Rhummel and Taforalt. Moreover, some early
African individuals have severe pathological alterations of
the vault that could influence the study of their endocranial
shape. In addition, some specimens that are sometimes
called archaicH. sapiens have morphological differences
with trueAMH (e.g., [23]). Therefore, we have not
considered specimens from these two groups in our study
(e.g., Eliye Springs, Jebel Irhoud, Florisbad, Ngaloba,
2 Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
Omo 2, Singa). In Asia, complete fossil skulls are rare. Some
questions have been raised about the antiquity of the speci-
mens from Liujang [24] and Zhoukoudian Upper Cave,
whereas the Wajak fossil is dated to <8,000 BP [25]. Simi-
larly, the chronology of the Australian specimens is debated,
even though some of them are definitely ancient. However,
the fossils from Coobool Creek, Kow Swamp, Lake Mungo,
Naccurie and Willandra Lake cannot be considered in this
study for various reasons such as incomplete preservation,
availability of endocranial casts and intentional cranial
deformation [26,27]. In the Levant, the Skhul and Qafzeh
sites have delivered a large number of fossils, including
some well-preserved skulls. Skhul V and Qafzeh 6 are
well-preserved and are included in this study. These are the
oldest specimens, aged 80,000 and 92,000 years respec-
tively. Finally, European specimens have been more closely
scrutinised in the past as more material was available, and
more accessible to some extent, as well as being well-pre-
served. A large number of Upper Pleistocene endocasts have
therefore been exhaustively investigated. This is the case, for
example, of Cro-Magnon 3, Predmostí 3, 4, 9 and 10, Brno
3, Dolní Vĕstonice 1 and 2, from the oldest to the most
recent specimen [1], or Cioclovina [28]. The ages of these
specimens range from 35,000 to 25,000 years. Unfortu-
nately, no information is available as yet about the endocast
of Peştera cu Oase 2 [29], which is currently the oldest
known directly dated well-preserved specimen, with an age
of 35,000
14
C BP [30]. Cro-Magnon 1, with an age of c.
28,000 years [17], is therefore one of the oldest nearly
complete endocasts of European fossil H. sapiens available
to date, but it has never been described as yet.
The fossil remains discovered in the Cro-Magnon site
are stored in the collections of the Musée de lHomme in
Paris, France. The skull of Cro-Magnon 1 (Fig. 1) was
scanned with a 16-row CT scanner (LightSpeed 16; Gen-
eral Electric Medical Systems, Milwaukee, Wisconsin)
[31]. Settings were 120 kV, 250 mA, 0.625-mm-thick
slices, reconstruction interval of 0.4 mm, 23 cm field of
view, 0.45 mm pixel size, 512 × 512 pixel matrix. Multi-
planar reformatting, thresholding procedures, 3D volume
rendering and metric analyses were performed with Arte-
Core 1 (NESPOS) and Avizo 7 (VGS). The boundary
between the bone and the air as well as the limits of the
different structures analysed were identified by manual
segmentation. This protocol required the use of multiple
threshold values as a function of variations in bone miner-
alisation. These settings enabled us to obtain precise
outlines and limits of the endocranial cavity and of all
Fig. 1 Anterolateral view of the original skull of Cro-Magnon 1; top row: illustration of its paranasal and temporal bone pneumatisa-
tion in the anterior and superior views, visible by transparency of the 3D model of the skull; the arrow indicates the position
of the pathological alteration on the frontal squama; bottom row: visualisation of the 3D reconstruction of the virtual endocast, visible
by transparency of the skull; physical replica of the endocast of Cro-Magnon 1 (A colour figure may be viewed in the online issue) /
Vue antérolatérale du crâne original de Cro-Magnon 1 ; la flèche indique la position de laltération pathologique de lécaille fron-
tale ; ligne du haut : illustration de sa pneumatisation paranasale et de los temporal en vues antérieure et supérieure, visible par
transparence du modèle tridimensionnel du crâne ; ligne du bas : visualisation de la reconstruction tridimensionnelle de lendocrâne,
visible par transparence du crâne ; réplique physique de lendocrâne de Cro-Magnon 1 (une version en couleurs de la figure est dis-
ponible dans la version en ligne de larticle)
Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18 3
pneumatic cells corresponding to the different areas of
pneumatisation, to produce accurate 3D reconstructions
(see [32] for a complete discussion of the segmentation
protocol and [3335] for examples of applications to the
reconstruction of virtual endocasts). Finally, we printed a
3D prototype of the Cro-Magnon 1 endocast (Fig. 1). The
physical replica was used to produce classic descriptions
and metric analysis of the endocast.
Comparative samples include physical endocasts of the
collections of the Muséum national dHistoire naturelle in
Paris, France, and consist of several fossil AMH (Skhul V,
Qafzeh 6, Cro-Magnon 3, Predmostí 3, 4, 9 and 10,
Brno 3, Dolní Vĕstonice 1 and 2, from the oldest to the
most recent specimen) and 102 endocasts of extant mod-
ern humans. The endocranial anatomy of Cro-Magnon 2,
Mladeč1 and Pataud 1 was also analysed with virtual
models obtained from CT data. The 3D model of the Cio-
clovina endocast [28,36] was provided by Kranioti and
also obtained from CT data. The fossil sample therefore
comprises 15 fairly complete specimens ranging from
92 to 25 ka in age. Sex is unknown for most of the speci-
mens because of the absence of associated infracranial ele-
ments and therefore of independent indicators for sexual
identification. The individuals of the extant sample were
non-pathological adults. The sex is not known for all the
specimens of the sample, but the sex ratio is probably
biased as this collection seems to comprise more males
than females, at least for specimens whose sex is known.
Most specimens are from recent historical times, with the
majority from the last two centuries. The geographic ori-
gin of the specimens is diverse, as they include 39 Eur-
opeans, 24 from the Pacific area, 15 Africans, 13 Asians
and 8 native Americans.
Methods
Morphology and morphometry of the endocast
Classic metric measurements using sliding and spreading
callipers were performed on the physical endocasts, on
virtual models with dedicated software (ArteCore and
Avizo) and on drawings for dimensions quantified in pro-
jections. Values for Cro-Magnon 1 were obtained from the
physical prototype obtained from the 3D reconstruction
(Fig. 1). These measurements quantify the lengths, heights
and widths of different areas of the endocast (Fig. 2 and
Table 1, please refer to [1,37] for a complete description
of the method).
The frontal, parietal and occipital chords were also
quantified based on anatomical landmarks related to brain
structures. The limit between the frontal lobes located ante-
riorly and the parieto-temporal lobes located posteriorly
corresponds superiorly and medially to the junction of the
central sulci and inferolaterally to the course of the small
depressions towards the upper part of the Sylvian valley.
This limit runs posteriorly to the coronal suture in a different
direction, getting closer to the suture while approaching the
Sylvian valley. The limit between the parieto-temporal
lobes located anteriorly and the occipital lobes located
posteriorly corresponds medially to the parieto-occipital
sulcus, which is frequently identifiable anteriorly to the
endo-lambda, and laterally to the pre-occipital notch. Over-
all, this limit follows the direction of the lambdoid suture but
does not correspond exactly to its course. Imprinting of these
sulcal impressions on fossil hominins is variable. They were
identified and observed on the physical endocasts with graz-
ing light and on the virtual models with virtual grazing light.
A complete description and definition of the sulcal impres-
sions is detailed elsewhere [1]. Figure 2 illustrates the posi-
tion of these sulci and of the lobes they delimitate as well as
of the major anatomical features described in this study.
Finally, we also measured the surface of the frontal,
parieto-temporal, occipital and cerebellar lobes [1,38]. The
limits of the lobes were defined by drawing continuous sulci
around closed areas (see [1] for a complete description of the
methodology). These limits between the different lobes were
distinguishable with enough confidence to be recognized
independently by two of us. The coordinates of 3D land-
marks (Fig. 2 and Table 1) forgeometric morphometric anal-
yses were registered with a microscribe [37]. However, the
incomplete preservation of the fossil specimens prevented a
detailed geometric morphometric comparison between the
fossil and extant samples. These landmarks are also useful
to define linear measurements (Fig. 2 and Table 1). Different
morphometric and statistical procedures were applied to ana-
lyse the recorded data, using PAST 2.11 software [39]. Lin-
ear regressions were performed with the Reduced Major
Axis algorithm [40], which minimises errors in both vari-
ables [41], and were used to investigate possible allometric
effects in the recorded data. All morphometric data were
scaled relatively to each individuals endocranial volume in
order to limit bias in global brain size variation between
samples. The cube-root of the endocranial volume (EV) for
each individual was thus used for size correction for each
linear variable ((xi/(3EVi)*100)) or for surface quantifica-
tion ((2xi)/(3EVi)*100)). The coefficient of variation
(CV = SD/mean) was corrected for small sample size using
the parameter V* (Table 2), which is calculated as V*
= [(1 + 1/4N) × CV] [42,43]. The permutation t-test was
preferred to the classic t-test to compare means for the fossil
and extant AMH. This test uses the t-statistic but is non-
parametric and is useful for comparing samples with non-
normal distribution and of unequal size. The sequential Bon-
ferroni procedure was used to correct for multiple tests
[44,45].
4 Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
Mapping the asymmetries of the endocast
The asymmetries of the endocranial surface of Cro-Magnon 1,
represented by a triangular mesh, were assessed through a
three-step automated method:
computation of the approximate plane of symmetry of the
surface [46];
computation of the 3D deformation field that allows the
nonlinear registration of the endocranial surface with
itself after mirror-flipping along its approximate plane of
symmetry [47];
and decomposition of each vector of this 3D deformation
(subsequently termed asymmetry) field into its 3 scalar
coordinates in a right-handed Cartesian coordinate system
consisting of the leftright, vertical and posterioranterior
axes.
Steps 1 and 2 were performed in a common statistical
framework in which the mesh was modelled using a mixture
of Gaussian probability density functions, and the points of
the flipped mesh were considered as samples drawn inde-
pendently according to this mixture; the plane of symmetry
and field of asymmetry were considered as unknown para-
meters of the Gaussian mixture and were estimated using the
maximum likelihood (ML) and the maximum a posteriori
(MAP) principles, respectively; the ML and MAP estima-
tions were performed using the Expectationmaximization
(EM) algorithm [48].
The decomposition of each vector of the asymmetry field
in an anatomy-based coordinate system allows a better inter-
pretation of the asymmetric field: the posterioranterior (PA)
component shows whether one side protrudes more towards
the front or the rear than the other, the vertical (top to bot-
tom) component shows whether one side is higher or lower
than the other, and finally the lateral (left to right) component
shows whether one side is more or less laterally extended
than the other with respect to the approximate computed
plane of symmetry.
Description of the internal cranial anatomy
of Cro-Magnon 1
The external cranial anatomy of the specimen has been pre-
viously detailed by others [5,6,10,11]. However, the imaging
dataset revealed that the internal structure of the bone is very
well-preserved which previously allowed the quantification
of cranial vault, tabular table and diploic layer thicknesses
[32], as is the endocranial surface of the specimen.
Pneumatisation
The complete extension of the frontal sinuses is preserved,
except for the lowest part just above the frontoethmoidal suture
Fig. 2 Three-dimensional model of the endocast of Cro-
Magnon 1 in the right lateral, superior and anterior views showing
the location of the landmarks and the measurements used to quan-
tify the endocranial anatomy (the full list and definitions are given
in Table 1) and the location of some analysed features (ss: sagittal
sinus, ts: transverse sinus, sis: sigmoid sinus, mv: meningeal ves-
sels, g: granular foveolas, cs: central sulcus, ls: lateral sulcus, is:
interparietal sulcus, pn: pre-occipital notch, afg: ascending frontal
gyrus, apg: ascending parietal gyrus, sg: supramarginal gyrus; see
[1] for all illustrations and definitions) / Modèles tridimensionnels
de lendocrâne de Cro-Magnon 1 illustrant la position des repères
anatomiques et les mesures utilisées pour quantifier lanatomie
de lendocrâne (leur liste complète et leur définition sont présen-
tées dans le Tableau 1) et la position de caractères anatomiques
(ss : sinus sagittal ; ts : sinus transverse ; sis : sinus sigmoïde ;
mv : système méningé moyen ; g : granulations de Pacchioni ;
cs : sulcus central ; ls : sulcus latéral ; is : sulcus interpariétal ;
pn : scissure préoccipitale ; afg : gyrus frontal ascendant ; apg :
gyrus pariétal ascendant ; sg : gyrus supramarginal ; et voir [1]
pour lensemble des définitions et des représentations)
Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18 5
(Fig. 1). The sinuses are large, particularly on the left side,
extending laterally above the orbital roof and posteriorly in
the frontal squama. They are fan-shaped from their base
towards their uppermost extension where the cells become
individualised. The cells are separated by very thin septa, as
are the two sinuses. A large and circular pathological alteration
is visible on the external surface of the right side of the frontal
squama, where it has deeply eroded the bone. As a result, the
right frontal sinus is separated from the bottom of the lesion
by a very thin layer of bone. Sphenoidal pneumatisation is
complete except for its anterior extension. The left sinus is
slightly larger than the right sinus. Most of the shape of the
maxillary sinuses is discernible but their upper and medial lim-
its as well as the lateral extent of the left sinus are altered due to
Table 1 Definition of the landmarks and the measurements used to quantify endocranial variations between fossil and extant anatom-
ically modern Homo sapiens (see Fig. 2 and refer [1,37] for a complete description of the method) / Définition des points repères
et des dimensions utilisés pour quantifier les variations de lendocrâne entre les échantillons fossile et récent dHommes anatomique-
ment modernes (voir Fig. 2 et lire [1,37] pour une description complète de la méthode)
Landmarks Definition
1 Base of encephalic rostrum between left and right first frontal convolution in the midsagittal plane
2 and 18 Left and right external edge of the encephalic rostrum
3 and 19 Left and right orbital part of the 3rd frontal convolution
4 and 20 Left and right point of maximal curvature of triangular part of the 3rd frontal convolution
5 and 21 Left and right upper point of the Sylvian valley
(between the opercular part of the 3rd frontal convolution and the temporal lobe)
6 and 22 Left and right most anterior point of the temporal lobe (temporal pole)
7 and 23 Left and right euryon (corresponding to the maximal endocranial width, MWE)
8 and 24 Left and right point of maximal curvature of the supramarginal gyrus
9 and 25 Left and right anterior point of the interparietal sulcus (base of the 1st parietal convolution)
10 and 26 Left and right middle point of anterior edge of the 1st parietal convolution
11 Intersection between the postcentral sulci and the interhemispheric fissure
12 and 27 Left and right upper point between the temporal and cerebellar lobes
(upper point of temporo-cerebellar excavation)
13 and 28 Left and right point of maximal curvature of the occipital lobe (occipital pole)
14 Posterior interhemispheric point (most depressed point of the torcular herophili)
15 Intersection between the left and right perpendicular sulci and the interhemispheric fissure
16 Intersection between the central sulci and the interhemispheric fissure
17 Middle point of the frontal chord
Dimensions Definition
MLE Maximal length
MWE Maximal width (between 7 and 23)
WSE Maximal width measured on the supramarginal gyri (between 8 and 24)
WPfE Maximal width measured on the foot of the 2nd parietal convolutions
WBcE Maximal width measured on Brocas cap (between 4 and 20)
WOfE Maximal width measured on the orbital part of the 3rd frontal convolutions (between 3 and 19)
WFfE Maximal width measured on the foot of the 3rd frontal convolutions
Wcereb Maximal width of the cerebellar lobes
BBHE Endobasion-endobregma height
BVHE Endobasion-endovertex height
MHlE Maximal height above the maximal length
BHlE Height of endobregma above the maximal length
FalC Frontal chord (between the base of encephalic rostrum and the intersection between the central sulci
and the interhemispheric fissure)
PalC Parietal chord (between the intersection between the central sulci and the interhemispheric fissure
and the intersection between the precentral sulci and the interhemispheric fissure)
OalC Occipital chord (between the intersection between the precentral sulci and the interhemispheric fissure
and the posterior interhemispheric point)
6 Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
bone loss in the orbital floor, the lateral walls of the nasal cavity
and part of the left maxillary arch. The sinuses are very similar
in size and shape on both sides. Finally, temporal bone pneu-
matisation fills the mastoid process as well as the upper part of
the petrous portion and has propagated slightly towards the rear
and above the external auditory meatus.
Description of the endocranial anatomy
of Cro-Magnon 1
Overall morphology
The entire cerebral surface is preserved, except for very
small portions with incomplete bone preservation corre-
sponding to the medial half of the left orbital lobe including
the area posterior to the encephalic rostrum, and a small
area at the medial course of the left central sulcus because
of sediment incrustations that could not be removed virtu-
ally with sufficient precision (Fig. 2). Sulcal impressions
and meningeal vessels are easily discernible thanks to the
remarkably well-preserved endocranial surface. The endo-
cast is ovoid in shape in the superior view. Its maximum
width is in the medial part of the supramarginal gyri. The
sagittal curvature is regularly convex in the lateral view.
Vascular impressions
Concerning the venous sinuses, there is no evidence of the
sphenoparietal sinuses. The superior sagittal sinus is visible
between the frontal lobes where its width increases antero-
posteriorly as far as the granular foveolas located in the pos-
terior part of the first frontal convolutions. The relief of the
sinus is less apparent posteriorly and again clearer from the
granular foveolas located in the upper part of the ascending
parietal gyri to the posterior extent of the parietal lobes. The
sinus deviates laterally to the right into the right transverse
sinus. This latter sinus deviates slightly in the direction of the
right cerebellar lobe. The width of the sinus increases along
its course. The right sigmoid sinus is in marked relief. The
left transverse sinus appears in the area of the confluence of
the sinuses. Its width and relief are less marked than on the
right side.
Concerning the meningeal vessels, the common tract of
the middle meningeal system is obvious on both sides on the
inferior surface of the temporal lobes from where it enters
the skull through the foramen spinosum. The middle menin-
geal system shows a similar pattern on both hemispheres.
The common tract splits into three unequal branches on the
superior temporal gyrus close to the temporal pole. The most
anterior branch corresponds to the anterior branch of the
middle meningeal system. This imprint is very short, disap-
pears in the area of the Sylvian valley on the left hemisphere
and shows some ramifications on the third frontal convolu-
tion on the right side. The largest branch runs vertically and
splits into two equal rami at the temporal fossa. The corre-
sponding anterior (or bregmatic) ramus runs close to the cor-
onal suture with short anterior ramifications towards the
frontal lobes and longer ramifications posteriorly that reach
the mid-sagittal area of the endocast. The posterior (or obe-
lic) ramus runs along the lateral sulcus on the parietal lobe.
Some anastomoses appear in the area of the angular gyrus.
Finally, the posterior (or lambdatic) branch arising from the
common tract runs horizontally as far as the inferior tempo-
ral gyrus, then upwards close to the temporocerebellar val-
ley. This branch splits into two rami that reach the upper part
of the temporal lobe and the occipital lobe respectively,
where both show some ramifications. This posterior branch
has longer rami with more ramifications on the right hemi-
sphere, and an obelic branch that joins the obelic branch
originating from the bregmatic branch, where they form a
number of anastomoses. Therefore, the anterior ramus cov-
ers the posterior part of the frontal lobe and nearly the whole
parietal lobe, being more developed than the posterior ramus
on the left hemisphere. The anterior ramus extends from the
ascending frontal gyrus to the supramarginal gyrus, whereas
the angular gyrus is covered by the posterior ramus on the
right hemisphere. These two rami are equally developed on
the right side.
Sulcal and gyral imprints
On the frontal lobes, the transverse curvature is regularly
convex in the anterior view, except where granular foveolas
form a bulky relief in the interhemispheric area. This curva-
ture is more circular at the level of the coronal suture and is
flattened on both sides more anteriorly. The encephalic ros-
trum is very short and wide, with a small inferior projection.
The right side of the rostrum is more convex and seems to be
projected more anteriorly. The course of the precentral sul-
cus is not easily discernible, and might correspond to the
depressed area situated behind the imprint left by the coronal
suture. The width of the ascending frontal gyri is estimated at
25 mm. Short and deep depressions clearly delimit the three
frontal convolutions on both sides. The relief on the third
frontal convolution is more clearly delimited on the left
side. The corresponding area on the right side has more dif-
fuse borders and seems larger. The ascending and anterior
rami delimit the triangular part on both sides. The latter is
depressed by the cap incisure on the left hemisphere. The
bulge in the area where the Brodmann area 45 would be
located is in its inferior part and separated from the temporal
pole by a very narrow space, particularly on the right side
where the frontal and temporal lobes are almost in contact.
The Sylvian valley is continued posteriorly by a clearly
Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18 7
visible lateral sulcus on both sides. The course of these sulci
is linear and almost horizontal.
Concerning the temporal lobes, their height on both sides
is identical from the pole to the parietooccipital sulcus. The
superior temporal sulcus is the least apparent but it clearly
delimits the superior temporal gyrus on both sides. Short and
deep depressions clearly delimit the middle and inferior tem-
poral gyri. The fourth and fifth temporal gyri are delimited
along their whole length by several depressions. These two
last sulci converge towards the pole on the left lobe and are
parallel on the right lobe. The upper part of the left temporal
pole is less voluminous than on the right side.
On the parietal lobes, the transverse curvature is very angu-
lar with the more lateral projecting points situated at the
supramarginal gyri: the curvature is regularly convex from
the base of the temporal lobes to the upper part of the inferior
parietal gyrus. It then becomes concave due to a wide and
shallow depression in the area of the interparietal sulcus.
The superior parietal gyri form a wide and large bulge,
where the relief of the superior sagittal sinus is visible all
along the parietal lobes. Many granular foveolas are visible
on both sides of this sinus. The central sulcus is not clearly
discernible in its uppermost extension. Its medial part clearly
delimits the ascending parietal gyrus from its base to the level
of the superior parietal gyrus on both sides. The central and
postcentral sulci are therefore discernible and their uppermost
extension could therefore be determined. The width of the
ascending parietal gyri is estimated at 25 mm. The interpar-
ietal sulcus is more obvious on the right side. The interparietal
sulci delimit the superior parietal gyri whose width decreases
anteroposteriorly. The borders of the supramarginal gyri are
clearly discernible. This gyrus is circular in shape and
markedly convex. The primary intermediate sulci form a shal-
low depression. The angular gyrus has a more apparent ante-
rior limit on the right side but the angular gyri are in clear
relief on both sides. The anteroinferior portion of the inferior
parietal gyrus forms a circular swelling of similar size on both
sides. The parieto-occipital sulcus is only apparent from the
pre-occipital notch on both sides.
The occipital lobes are below the parietal lobes and the
sagittal curvature at the junction of these lobes is regularly
convex in the lateral view. The occipital lobes have a slight
posterior projection and are triangular in shape. The three
occipital gyri are clearly discernible on the right side whereas
only the inferior occipital sulcus is visible on the left side.
The cerebellar lobes are below the temporal and occipital
lobes, in a posterior position relatively to the cerebrum, and
are ovoid in shape. The horizontal sulcus is formed by small
depressions on both hemispheres. The interhemispheric
space is wide. The space between the temporal and cerebel-
lar lobes is wider on the left side. The narrower space on the
right side is due to the larger size of the posterior part of the
inferior temporal gyrus and to a larger sigmoid sinus on this
side compared to the left side.
Endocranial asymmetries
A pattern of right frontal-left occipital petalia (following the
definition and methodology of [49]) is visible on this endocast
(Fig. 3). Moreover, the right frontal pole is located 1.8 mm
anteriorly to the left pole and the left occipital pole projects
1.1 mm behind the right one (following the definition and
methodology of [50]). The left occipital lobe also protrudes
medially on the right side of the mid-sagittal plane of the
endocast when viewed from the top. The hemispheric length
is approximately equal on both sides (R: 182 mm,
L: 180 mm). The width of the frontal lobes is nearly the
same on both hemispheres, whereas the area of the left parie-
totemporal lobe is larger on the left side. Various quantified
heights are equal on both sides. The supramarginal and angu-
lar gyri are well delimited and their relief is similar on both
sides (Fig. 3). The bulge in the area where the Brodmann area
45 would be located is larger on the right side, thus narrowing
the Sylvian valley. In this area, the anterior and posterior rami
of the central sulcus are clearer on the left hemisphere. The
middle meningeal system, including the distribution of the
ramifications and anastomoses, displays a similar pattern
and development on both hemispheres (Fig. 3).
We were also able to quantify the asymmetries of the
whole endocast by comparing its right and left sides. We
divided the observed bilateral variation into three components
in order to characterise the asymmetries in the three dimen-
sions separately (Fig. 4). Width differences (X axis, or lateral
variation) are particularly noticeable on the temporal lobes
(towards the right except for the posterior part of the inferior
temporal gyrus, which is more laterally projected on the left
side) and in the area of the first frontal gyrus and the superior
parietal gyrus (towards the left). The areas corresponding to
the occipital poles have a more lateral extension on the right
side than on the left side and the left side seems to bend
towards the right. The most pronounced vertical asymmetries
(Y axis) concern the first frontal gyrus and the superior parie-
tal gyrus (the left side being higher than the right side) as well
as the posterior part of the inferior temporal gyrus and the
lower part of the occipital lobe (the right side being higher
than the left side). Finally, variations in anteroposterior layout
(or protrusions, Z axis) show that the right hemisphere has a
more anterior position overall compared to the left hemi-
sphere, particularly in the anterior part of the frontal lobes
and temporal lobes, the posterior part of the inferior parietal
gyrus and the occipital lobe.
The pattern of asymmetry of this endocast may therefore
be summarised as follows (refer to the areas in darker
colours on Figs 4, 5). The pattern of right frontal-left occipi-
tal protrusion is confirmed. The anterior part of the frontal
8 Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
lobes is asymmetric only in the anteroposterior component,
the right hemisphere being more anteriorly projected than
the left one. The right occipital lobe (and its pole) is also
more anterior than its counterpart on the other side, but
is also in a more elevated position and more laterally
expanded. The first frontal gyrus is asymmetric in its poste-
rior half, as is the uppermost extension of the ascending fron-
tal gyrus, the corresponding left gyri being more developed
vertically and laterally than on the right side. The most
asymmetric area of the parietal lobes is the superior parietal
gyrus, which is higher and wider on the left hemisphere. The
whole temporal lobe projects more laterally on the right side
and also has a more anterior position.
Comparative analyses of endocranial anatomy in
H. sapiens
A comparison between fossil and extant H. sapiens is possi-
ble thanks to previous results [1] and to the original results
and synthesis proposed here, which focus on features of
Fig. 3 Line drawings of the endocast of Cro-Magnon 1 in the superior, right lateral, anterior, posterior and left lateral views; drawings
by P. Hervé / Dessins de lendocrâne de Cro-Magnon 1 en vues supérieure, latérale droite, antérieure, postérieure et latérale gauche ;
dessins de P. Hervé
Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18 9
interest for the study of hominin evolution and/or features
that vary among AMH.
Vascular impressions
The superior sagittal sinus deviates into the right transverse
sinus on all the fossil AMH where this region is preserved
(Predmostí 3, 9, 10, Brno 3, Dolní Vĕstonice 2, Cro-
Magnon 1, 3, Cioclovina) and on 80% of the extant humans.
The right lateral sinus is larger and more marked than on the
left on all the endocasts studied. No sphenoparietal sinus is
observed among the 102 extant humans, and only Cro-
Magnon 3 and Brno 3 exhibit a moderate relief in the corre-
sponding area.
The middle meningeal system follows a similar pattern
both on extant humans and the fossil AMH, with a predomi-
nant anterior ramus consisting of the bregmatic and obelic
meningeal branches. The obelic branch has a double origin
(from the bregmatic branch and from the lambdatic branch)
on both hemispheres of Predmostí 3, on the right hemisphere
of Predmostí 4 and on the left hemisphere of Dolní Vĕsto-
nice 1 and 2. The anterior ramus is always more developed
than the posterior (lambdatic) one, which is small on all the
fossil AMH. The same pattern is observed in 80% of the
extant humans, 12% of which have anterior and posterior
branches with equivalent development. The anterior ramus
covers the cerebral surface from the posterior region of the
frontal convolutions to the angular gyrus on both sides on
the extant humans, Cro-Magnon 3, Predmostí 10 and on the
left hemisphere of Predmostí 9. On both sides on Cro-
Magnon 1, Dolní Vĕstonice 1 and 2, Brno 3, Predmostí 3,
4, and on the right hemisphere of Predmostí 9, the anterior
ramus is slightly less developed and reaches the supramar-
ginal gyrus, and the angular gyrus is covered by the posterior
ramus. The general orientation of the middle meningeal
imprints is oblique. The ramifications are numerous and
joined by a number of anastomoses that form a covering
pattern. The ramifications and anastomoses are less numer-
ous on fossil AMH than on extant humans.
Sulcal and gyral imprints
Formed by the extremities of the left and right first frontal
convolutions, the encephalic rostrum is short and wide on
the fossil AMH and on the extant humans. The left convolu-
tion is wider on Predmostí 10, Cro-Magnon 3 and on 40% of
Fig. 4 Illustration of bilateral asymmetries of the endocast of Cro-Magnon 1 in the anterior, right lateral, posterior, superior and inferior
views, from left to right, in their lateral (X), vertical (Y) and posterioranterior (Z) components. The chromatic scale highlights differ-
ences (from left to right sides of the scale) in lateral extension towards the left/right, vertical differences from bottom to top and horizontal
differences from back to front (Colour figure may be viewed in the online issue) / Illustration des asymétries bilatérales de lendocrâne
de Cro-Magnon 1 en vues antérieure, latérale droite, postérieure, supérieure et inférieure, de gauche à droite, détaillées dans leurs
composantes latérale (X), verticale (Y) et antéropostérieure (Z). Léchelle chromatique illustre (de la gauche vers la droite de léchelle)
des différences latérales vers la gauche/droite, des différences verticales du bas vers le haut et des différences horizontales de larrière
vers lavant (une version en couleur de la figure est disponible dans la version en ligne de larticle)
10 Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
the extant humans. The right frontal convolution is wider on
Predmostí 4, 9, Dolní Vĕstonice 1, 2, Cro-Magnon 1, Cio-
clovina and on 41% of the extant humans. The width of the
extremities of these first frontal convolutions is identical on
Predmostí 3 and on 19% of the extant humans. The left and
right frontal hemispheres are nearly joined, separated only
by a deep and narrow interhemispheric sulcus on all the
endocasts studied. The frontal relief is marked and well
delimited, especially on the third frontal convolution. The
triangular part is perfectly delimited and more prominent
and more bulging on the left hemisphere on Predmostí 4,
Cro-Magnon 1, 3, Cioclovina and Dolní Vĕstonice 1. Incom-
plete preservation prevents comparison with the other fossil
specimens. The left triangular part is also more developed on
72% of the extant humans (16% on the right lobe and 12%
equal). The triangular part is depressed on all of them by the
cap incisure. The triangular part is very close to the temporal
pole, just separated by a narrow Sylvian valley. The frontal
and temporal lobes are nearly joined. Posteriorly, the lateral
sulcus is always deeply imprinted. It is rectilinear and nearly
horizontal, and longer and deeper on the left hemisphere
compared to the right.
The parietal gyri are well delimited, especially the large
and convex first parietal convolution where the lower part is
limited by the depressed interparietal sulcus. The relief on
the second parietal convolution is also well marked, as is the
supramarginal gyrus, which has a rounded shape. The bulge
is more prominent on the left parietal lobe on Predmostí 3,
Brno 3, Cro-Magnon 3 and Dolní Vĕstonice 2 than on 41%
of the extant humans. The relief is more developed on the
right parietal lobe on Predmostí 10 and on 37% of the extant
humans. It is equally developed on both hemispheres on Pre-
dmostí 4, 9 and on 22 % of the extant humans.
The temporal sulci are parallel. On the fossil specimens,
there is a wide space between the posterior part of the tem-
poral and cerebellar lobes, which are located under the pari-
etal and occipital lobes. The hemispheres and the cerebellar
lobes are closer on extant humans, and the cerebellar lobes
are in a more anterior position.
The occipital lobes on all the endocasts are in an anterior
position, below the parietal lobes. They are widely separated
on the fossil AMH and closer on extant humans: they are
joined together in 30% of the specimens, separated by a
deep and narrow fissure in half of the specimens and by a
wider fissure in the remaining individuals.
Morphometric analyses
The different dimensions quantified on the Cro-
Magnon 1 endocast are within the range of variation
observed in our sample of fossil modern humans. Therefore,
we included Cro-Magnon 1 in the sample of fossil AMH (N
=815 depending on the variable analysed and the state of
preservation of the specimens) and compared the latter sam-
ple with the sample of extant modern humans (N = 102).
The first important observation from this study concerns
the endocranial volume. This volume is absolutely and sig-
nificantly smaller in extant H. sapiens compared to the fossil
sample (p<0.001). Moreover, a mean value of 1,350 cm
3
(SD = 77.5) was quantified on a sample of 20,000 recent
skulls from all over the world, with some populational and
geographic variations and sexual dimorphism [51]. Mean
cranial capacity was 1,427 cm
3
(SD = 81.6) for males and
1,272 cm
3
(SD = 82.9) for females. The mean endocranial
volume for a sample of 28 fossil specimens dated from
Fig. 5 Illustration of the magnitude of the asymmetry vector made of the three components for the endocast of Cro-Magnon 1 and sche-
matic superposition of Brodmann areas (Colour figure may be viewed in the online issue) / Illustration du vecteur de symétrie combinant
ses trois composantes pour lendocrâne de Cro-Magnon 1 et superposition schématique des aires de Brodmann (une version en couleur
de la figure est disponible dans la version en ligne de larticle)
Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18 11
190,000 to 25,000 years, for which endocranial volume is
documented [2], is 1,478 cm
3
. The value obtained for our
more limited fossil sample (N = 13) is 1,514 cm
3
(SD = 137.9). We do not have information on sex for the
entire fossil sample but there is no reason to assume any
significant over-representation of males and therefore any
significant overestimation of the mean endocranial volume
due to a sexual bias in the composition of the sample. Over-
all, these results suggest a decrease in endocranial volume
between fossil AMH and recent humans, whatever their geo-
graphic origin [51].
For this reason, all data were scaled relatively to individ-
ual endocranial size in order to facilitate further comparisons
between samples (Tables 24). Moreover, linear regressions
between endocranial size and the scaled data for each quan-
tified measurement were performed to detect any allometric
relationships among the recorded morphometric data. For all
the variables, the coefficient of regression was very low and
the relationship was always non-significant.
The morphometric comparison between the fossil and
extant samples brought out many common features, but
also some significant relative metric differences (Table 2).
The fossil sample is within the range of variation observed
in the large sample of extant modern humans in most of the
specimens analysed for morphometric data (Tables 24).
Hotellings T-squared test was used to test for differences
between the fossil and extant samples, which are signifi-
cant (p<0.001) when all the morphometric data are consid-
ered globally. Geometric morphometric analyses could
not be performed on a large fossil sample because of the
incomplete preservation of the specimens. A geometric
morphometric test showed that the fossil specimens,
including Cro-Magnon 1, were projected in the variation
of the extant sample.
In more detail, the maximum length of the endocast
(MLE) is significantly greater in the fossil sample (noted
fossil AMH below) compared to the extant sample (noted
extant AMH below) (15.9 versus 14.9, p < 0.001) and the
difference between these mean values is 7%. Endocranial
widths measured in different areas of the endocast (MWE,
WSE, WPfE, WBcE, WOfE and WFfE located on different
areas of the frontal and parietal lobes, Fig. 2 and Table 1)
Table 2 Morphometric results for linear distances / Résultats morphométriques pour les distances linéaires
EV
(cr)
MLE MWE WSE WPfE WBcE WOfE WFfE Wcereb BBHE BVHE MHlE BHlE
fossil
AMH
N 1513141514129 119 9 8 1112
V* 2.9 3.9 4.3 4.9 4.8 4.6 3.3 5.3 5.6 4.0 4.6 7,9 5,9
Min 10.8 15.1 10.8 10.7 10.7 8.7 7.1 9.2 9.0 10.3 10.6 6,0 5,5
Mean-SD 11.1 15.3 11.4 10.9 10.9 8.8 7.2 9.5 9.1 10.6 10.7 6,2 5,6
Mean 11.5 15.9 11.9 11.4 11.4 9.2 7.5 10.1 9.7 11.0 11.2 6,8 6,0
Mean+SD 11.8 16.5 12.3 12.0 12.0 9.7 7.7 10.6 10.2 11.4 11.7 7,3 6,3
Max 12.0 17.0 12.9 12.5 12.5 10.0 7.9 10.9 10.6 11.8 12.2 7,8 6,5
Exta-
nt
AMH
N 102 102 102 102 102 102 102 102 102 101 101 101 101
V* 3.5 4.1 4.5 3.9 4.2 5.7 12.8 5.3 4.8 3.9 3.5 10,9 11,9
Min 10.6 13.5 10.6 10.3 10.2 8.1 5.9 8.8 8.1 9.2 9.9 4,6 4,1
Mean-SD 11.1 14.3 11.3 11.1 10.9 8.6 6.6 9.6 8.8 10.2 10.5 5,2 4,5
Mean 11.5 14.9 11.9 11.5 11.3 9.1 7.5 10.1 9.2 10.6 10.8 5,8 5,1
Mean+SD 11.9 15.5 12.4 11.9 11.8 9.7 8.5 10.7 9.7 11.0 11.2 6,4 5,7
Max 12.5 16.0 13.1 12.7 12.4 10.5 9.9 11.5 10.3 11.5 11.8 7,5 6,8
perm. t
(bc) p
ns *** ns ns ns ns ns ns * * * *** ***
%
MeanVar
0700110-15 431616
N: number of individuals; V*: coefficient of variation corrected for small sample size; metric results with size correction; perm. t(bc)
p: p value of the permutation t-test with sequential Bonferroni correction for multiple tests, * indicates a p-value < 0.05, ** p < 0.01,
*** p < 0.001; %MeanVar: percentage of variation between the means for fossil AMH and extant AMH samples; see Fig. 2 for illustra-
tion of linear distances and Table 1 for definitions (N : nombre dindividus ; V* : coefficient de variation corrigé pour des échantillons
de petite taille ; les données présentées ont été corrigées pour la taille ; perm. t(bc) p : valeur p du test t de permutation avec correc-
tion séquentielle de Bonferroni pour tests multiples, * indique une valeur de p < 0,05, ** p < 0,01, *** p < 0,001; %MeanVar :
pourcentage de variation entre les moyennes pour les échantillons fossile et récent dHommes anatomiquement modernes ; voir
la Figure 2 pour illustration des distances linéaires et le Tableau 1 pour leurs définitions).
12 Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
are not significantly different between the two samples.
The difference between the mean values for these variables
for the two samples ranges from 1 to +2%. Only the width
of the cerebellar lobes (Wecereb) is significantly greater in
fossil AMH (9.7 versus 9.2, p<0.05, difference of 5%).
Concerning endocranial heights, the different quantified
dimensions (BBHE, BVHE, MHIE and BHIE, Tables 1, 2)
are significantly larger in fossil AMH, with differences in
mean values ranging from 3 to 16%. Partial heights
above the maximum length of the endocast (MHIE and
BHIE) vary to a much larger extent between fossil AMH
and extant AMH (differences of 16%, p < 0.001) than do
total heights (BBHE and BVHE, differences of 34%,
p < 0.05).
The frontal chord and the occipital chord are significantly
larger in fossil AMH (p < 0.001) whereas the parietal chord
is significantly larger in extant AMH (p < 0.05, Table 3). In
relation to this pattern, the width of the ascending frontal
gyri (Wfas) and of the ascending parietal gyri (Wpas) are
significantly (p < 0.001) larger in fossil AMH (N = 12,
values of 1.94 for Wfas and 1.83 for Wpas) than in extant
AMH (N = 101, 1.27 and 1.29).
Finally, the surface of the frontal lobe is significantly
larger in fossil AMH (p<0.001), with a difference of 6%
between the mean values of the samples, as is the surface
of the occipital lobes (p<0.01) with a mean difference of
8%, whereas the surfaces of the parietal and temporal lobes
are not significantly different (Table 4). The surface of
the cerebellar lobes is significantly larger in extant AMH
(p<0.05), with a mean difference of 5%.
The difference in shape between fossil AMH and extant
AMH endocasts may therefore be described and sum-
marised as follows. While the overall shape of the endo-
casts does not differ noticeably in lateral extension, the
vertical and anteroposterior differences between the sam-
ples are significant. In extant AMH, the frontal lobes are
relatively shorter anteroposteriorly and their surface is
smaller. The parietal lobes are longer although the surface
of the parietotemporal lobes does not change. The occipital
lobes become shorter vertically and their surface is smaller.
This is related to an anteroposterior compression of the
endocast and to a vertical compression of its upper part,
where the width does not differ between fossil AMH and
extant AMH.
Table 3 Morphometric results for the frontal, parietal and occipital chords / Résultats morphométriques pour les cordes frontale,
pariétale et occipitale
FC PC OC Wfas Wpas
fossil AMH N 14 15 14 12 12
V* 4.03 6.79 8.11 18.67 12.15
Min 10.59 5.17 5.25 1.46 1.46
Mean-SD 10.88 5.60 5.47 1.58 1.61
Mean 11.33 6.00 5.94 1.94 1.83
Mean+SD 11.78 6.40 6.41 2.29 2.05
Max 12.16 6.92 6.80 2.75 2.18
Extant AMH N 102 102 102 101 101
V* 4.34 11.03 8.65 12.53 12.61
Min 9.48 4.58 4.12 0.83 0.83
Mean-SD 10.22 5.72 4.66 1.11 1.13
Mean 10.69 6.43 5.10 1.27 1.29
Mean+SD 11.15 7.14 5.54 1.42 1.46
Max 12.08 7.72 6.18 1.72 1.72
perm. t(bc) p *** * *** *** ***
%MeanVar 6 -7 16 51 40
N: number of individuals; V*: coefficient of variation corrected for small sample size; metric results with size correction; perm. t(bc)
p: p-value of the permutation t-test with sequential Bonferroni correction for multiple tests, * indicates a p-value < 0.05, ** p < 0.01,
*** p < 0.001; %MeanVar: percentage of variation between the means for fossil AMH and extant AMH samples; see Table 1 for defi-
nitions of linear distances (N : nombre dindividus ; V* : coefficient de variation corrigé pour des échantillons de petite taille ;
les données présentées ont été corrigées pour la taille ; perm. t(bc) p : valeur p du test t de permutation avec correction séquentielle
de Bonferroni pour tests multiples ; * indique une valeur de p < 0,05, ** p < 0,01, *** p < 0,001 ; %MeanVar : pourcentage de vari-
ation entre les moyennes pour les échantillons fossile et récent dHommes anatomiquement modernes ; voir le Tableau 1 pour la défini-
tion des distances linéaires).
Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18 13
Discussion
Cro-Magnon 1 and H. sapiens
Virtual anthropology, with specific constraints related to
the particular nature of the material analysed [52], is
undoubtedly a useful addition to the large analytical toolkit
available to researchers and curators. In the case of Cro-
Magnon 1, imaging and prototyping methodologies have
for the first time allowed the observation, reconstruction
and physical reproduction of endocranial anatomical fea-
tures (Fig. 1), which are helping to document the anatomy
of this important specimen [57].
Frontal pneumatisation is highly variable in both extant
(e.g., [53,54]) and fossil [17,32,55] H. sapiens. Cro-
Magnon 1 is within this range of variation, whereas differ-
ences in shape and extension are obvious in this species
compared with fossil hominins, and particularly Neander-
tals. However, as of now it is not clear whether the shape
and size of the frontal sinuses can be really helpful to phylo-
genetic discussions. Moreover, their role and function also
remain unclear [55,56]. Similarly, the pattern of temporal
bone pneumatisation in Cro-Magnon 1 is within the range
of variability described for H. sapiens, which differs to some
extent from the characteristics observed in other hominin
species [57,58]. Our previous works on temporal bone pneu-
matisation have shown that the development of pneumatisa-
tion does not play an active role in determining the morphol-
ogy of the temporal bone, and particularly the expression of
various apomorphic features of the different species. The
development of temporal bone pneumatisation is likely to
be principally related to available space and to the temporal
bone morphology. In this context, the shape and distribution
of the paranasal and temporal bone pneumatisation in Cro-
Magnon 1 correspond to what would be expected for H.
sapiens.
Finally, the endocranial morphology, including vascular,
gyral and sulcal characteristics, of Cro-Magnon 1 is within
the range of variation observed in H. sapiens [1], including
both extant and fossil samples, which exhibit some clear
differences with other hominin species [1,38]. However,
we have also identified a number of differences between
the sample of fossil AMH and our extant sample. These dif-
ferences are discussed in more detail below.
Table 4 Morphometric results for the surface of the frontal, parieto-temporal, occipital and cerebellar lobes / Résultats morphométri-
ques pour la surface des lobes frontaux, pariétotemporaux, occipitaux et cérébelleux
Frontal lobes Parietal lobes Occipital lobes Cerebellar lobes
fossil AMH N 11 7 10 7
V* 4.3 5.0 6.1 6.4
Min 109.9 133.7 68.6 62.6
Mean-SD 115.6 134.3 70.0 63.2
Mean 120.6 141.1 74.4 67.4
Mean+SD 125.7 147.9 78.9 71.5
Max 127.7 155.2 83.1 73.0
Extant AMH N 98 98 98 97
V* 4.0 2.9 8.0 5.4
Min 100.4 129.3 53.9 61.5
Mean-SD 109.3 136.1 63.2 67.3
Mean 113.9 140.2 68.7 71.1
Mean+SD 118.4 144.3 74.1 74.9
Max 125.1 150.3 80.4 78.9
perm. t(bc) p *** ns ** *
%MeanVar 6 1 8 -5
N: number of individuals; V*: coefficient of variation corrected for small sample size; metric results with size correction; perm. t(bc)
p: p value of the permutation t test with sequential Bonferroni correction for multiple tests, * indicates a p-value < 0.05, ** p < 0.01,
*** p < 0.001; %MeanVar: percentage of variation between the means for fossil AMH and extant AMH samples (N : nombre dindi-
vidus ; V* : coefficient de variation corrigé pour des échantillons de petite taille ; les données présentées ont été corrigées
pour la taille ; perm. t(bc) p : valeur p du test t de permutation avec correction séquentielle de Bonferroni pour tests multiples ; *
indique une valeur de p < 0,05, ** p < 0,01, *** p < 0,001 ; %MeanVar : pourcentage de variation entre les moyennes
pour les échantillons fossile et récent dHommes anatomiquement modernes).
14 Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
Endocranial asymmetries in H. sapiens
It was not possible to draw any firm conclusion on the pres-
ence of asymmetries at the populational level for fossil
H. sapiens because of the restricted sample available. Values
for Cro-Magnon 1 are larger than the mean values for the
sample of extant modern humans but are within their range
of variation. The largest asymmetry concerns the lateral
component of the occipital petalia (cf. Fig. 4). Asymmetric
areas are located in the anterior part of the frontal and tem-
poral lobes, in the upper extension of the frontal and parietal
lobes just laterally to the mid-sagittal plane, and concern the
occipital lobes (Figs 4, 5). Cro-Magnon 1 shows similar pat-
terns for all the components of endocranial petalia compared
with a sample of 45 extant modern humans [50].
Human brain asymmetries have been documented for over
a century and widely investigated for their functional, physi-
ological or behavioural implications. For example, the larger
frontal or occipital projection is usually coupled with a larger
lateral extent of the more projecting hemisphere relative to the
other. It is presently accepted that this pattern of asymmetry
appeared with early Homo [2,49,59,60] and is most common
in right-handed individuals [6167]. Brain asymmetries are a
topic in non-human primate studies [49,61,63,6873] and are
of special interest in paleoanthropology [1,2,49,59,60,74]
because of their relationships with right and left handedness
and, more generally, with specific aspects of human cogni-
tion, including language. However, the investigation of endo-
cranial asymmetries in the human fossil record has not yet
received the scrutiny it deserves. When all the available infor-
mation about overall of the brain asymmetry in modern
humans is considered, it appears that the left occipital lobe
is significantly larger in volume [75], surface [38] and in the
posterior extension of its pole [49,50] than the right occipital
lobe. In the meantime, the right frontal lobehas a significantly
larger volume [75], a non-significantly larger surface [37], a
non-significantly larger anterior extension of its pole [50] and
a more lateral extension [49]. Variations in morphology and
size of the anterior part of the frontal lobe are related to varia-
tions in surface, particularly of the anterior extension, and
probably to a lesser extent to variations in the volume of the
whole lobe. This set of evidence from various studies and for
different features shows that the occipital lobes exhibit a pat-
tern of significant directional asymmetry in favour of the left
side in the posterior extension at the population level in AMH,
whereas variations in the shape and dimensions of the fron-
tal lobes in our species seem to be mostly related to a pat-
tern of fluctuating asymmetry. These aspects remain to be
detailed from larger samples of fossil specimens, using new
methodologies that allow fine details about brain asymmetries
to be quantified. Recent results show that it is essential to
define asymmetrical traits of the surface of the brain correctly
by studying large populations with suitable methodologies.
The methodology described here, which quantifies areas and
directions of bilateral asymmetry, while remaining indepen-
dent of overall brain asymmetry, will certainly allow major
developments for the quantification of these features.
Morphometric evolution of the H. sapiens brain
In detail, the analyses of the size-corrected variation described
here show that the maximum length of the endocast is signifi-
cantly larger in the fossil sample compared to the extant sam-
ple (Fig. 6). The widths and surfaces measured on different
areas of the frontal parietal lobes do not differ significantly
between the two samples, except for the width of the cerebel-
lar lobes, which is significantly larger in Upper Pleistocene
AMH. The different quantified endocranial heights are signif-
icantly larger in the fossil AMH sample. The frontal chord
and the occipital chord are also significantly larger in the fos-
sil AMH sample, whereas the parietal chord is significantly
larger in the extant AMH sample. In relation to this pattern,
the width of the ascending frontal gyri and of the ascending
parietal gyri are significantly larger in the fossil AMH.
Finally, the surface of the frontal and parietotemporal lobes
are significantly larger in the fossil AMH, whereas the surface
of the parietotemporal lobes does not differ significantly and
the surface of the cerebellar lobes is significantly larger in the
extant AMH sample. Although significant, this difference
between the fossil and extant samples in the surface of the
different brain regions is smaller than the differences observed
between different species of the genus Homo [38]. Finally, we
have demonstrated that the various reported differences
between the fossil and extant samples were not correlated to
size-related effectsand not due to allometric effects: the linear
regressions between endocranial size and the scaled data for
each quantified measurement were all non-significantly
correlated.
A decrease in absolute endocranial size since the Upper
Pleistocene is noticeable in H. sapiens. Several hypotheses
have been put forward to explain this decrease, and are yet
to be fully explored. Although we cannot explain the ori-
gin of this variation as yet, we have also found that both
extant and older endocrania have the same anatomical lay-
out, but nonetheless show non-allometric differences in
the relative size and organisation of different parts of the
brain. Between the fossil sample and the extant H. sapiens,
there is an overall decrease in the volume, relative length
and height of the endocast, along with smaller frontal and
occipital lobes, while the width of the endocast and the
size of the parietal lobes has remained relatively stable
and, finally, a relative expansion of the cerebellar lobes
appears to have occurred (see also [76]). However, we
cannot conclude on the possible differences in functional-
ity of the brain related to these morphological variations
as there is no evidence to support a clear discontinuity
Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18 15
between the capacities of our predecessors, Palaeolithic
H. sapiens, and ours. The results we have obtained show
that the H. sapiens brain is very plastic, with some areas
(frontal and occipital lobes) being more adaptive than
others (parietal, temporal or cerebellar lobes), which may
be due to constraints on maintaining optimal performance
while reducing in size and changing in shape.
Conclusion
Developments in brain mapping and computational anatomy
in the last twenty years have expanded possibilities for ana-
lysing brain structure and function (e.g. [77]). Here we have
opened up a new perspective on knowledge of the anatomy
of the H. sapiens brain, whose recent evolution had never
before been investigated in the light of this feature, which
is clearly an important gap in scientific knowledge.
A decrease in absolute endocranial size has occurred
between fossil specimens and recent populations in H. sapi-
ens. This variation is also associated with noticeable non-
allometric variations in the relative size and shape of the
different areas of the brain of fossil and extant AMH,
which may be described and summarised as follows. The
overall shape of the endocasts does not exhibit noticeable
changes in width, but it does show substantial vertical
and anteroposterior variations. The frontal lobes have
become relatively shorter anteroposteriorly and their
surface has decreased. Parietal lobes are longer while the
surface of the parietotemporal lobes has not changed.
Occipital lobes have become shorter vertically and their
surface has decreased. This is related to an anteroposterior
compressionof the endocast and to a vertical compres-
sionof its upper part where its width does not differ
between fossil and extant AMH. As of now, these morpho-
logical variations of the brain during the recent evolu-
tion of our species are impossible to correlate with func-
tional data or interpretations of variations in human
capacities that have certainly not varied so widely over
time. This illustrates the complex correlation between
form and function and highlights the considerable plastic-
ity of the H. sapiens brain.
Fig. 6 Schematic representation in the right lateral view of the variations in endocranial anatomy between a fossil (external outline cor-
responding to Cro-Magnon 1) and a meanextant anatomically modern human (internal outline corresponding to a recent endocast
with quantified measurements made in this study that are close to the mean values for the extant AMH sample) (Colour figure may be
viewed in the online issue) / Représentation schématique en vue latérale droite de la variation morphologique de lendocrâne entre les
Hommes anatomiquement modernes fossiles (contour externe qui correspond à Cro-Magnon 1) et récents (contour interne qui corre-
spond à un endocrâne dHomme actuel dont les dimensions sont proches de la moyenne observée pour léchantillon pour toutes les vari-
ables analysées (une version en couleur de la figure est disponible dans la version en ligne de larticle)
16 Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
Acknowledgments : We are very grateful to the following
institutions and individuals for allowing us to study endo-
casts in their care: E. Kranioti, University of Edinburgh,
Scotland; A. Froment, P. Mennecier, H. de Lumley and
F. Sémah, Muséum national dHistoire naturelle, Paris,
France. We are also indebted to A. Fort and V. Laborde
for their help during the analysis of the endocast collec-
tion of the Musée de lHomme and to P. Hervé for the draw-
ings of the endocast of Cro-Magnon 1. This work has
benefited from earlier discussions with E. Gilissen of the
Royal Museum of Central Africa in Tervuren, Belgium.
The comments from two anonymous reviewers and Editor
in Chief E. Herrscher have greatly improved this paper.
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18 Bull. Mém. Soc. Anthropol. Paris (2013) 25:1-18
... However, the comparison with fossil hominins is complex for various reasons. Moreover, the question of the date of appearance of particular anatomical traits, including brain asymmetries, in the hominid lineage is still widely debated [25][26][27][28][29]. Among the aspects considered at this interface, the combination of right frontal/left occipital protrusions, usually associated with the 'torque' pattern, has been studied on brain endocasts (the imprints left by the brain on the internal surface of the skull), from both recent humans and fossil hominins. ...
... In a previous study [28], we demonstrated clear differences in brain organization when considering the relative contribution of the different lobes to the surface of the complete endocast. Asian H. erectus specimens show a significantly smaller relative size of the parietal and temporal lobes than all other samples of the genus Homo. ...
... In this context, there is little information available about variations in the global size of the different lobes and their relationship with each other between hominin species. In a previous study [28], we demonstrated clear differences in brain organization when considering the relative contribution of the different lobes to the surface of the complete endocast. Asian H. erectus specimens show a significantly smaller relative size of the parietal and temporal lobes than all other samples of the genus Homo. ...
Article
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We are interested here in the central organ of our thoughts: the brain. Advances in neuroscience have made it possible to obtain increasing information on the anatomy of this organ, at ever-higher resolutions, with different imaging techniques, on ever-larger samples. At the same time, paleoanthropology has to deal with partial reflections on the shape of the brain, on fragmentary specimens and small samples in an attempt to approach the morphology of the brain of past human species. It undeniably emerges from the perspective we propose here that paleoanthropology has much to gain from interacting more with the field of neuroimaging. Improving our understanding of the morphology of the endocast necessarily involves studying the external surface of the brain and the link it maintains with the internal surface of the skull. The contribution of neuroimaging will allow us to better define the relationship between brain and endocast. Models of intra- and inter-species variability in brain morphology inferred from large neuroimaging databases will help make the most of the rare endocasts of extinct species. We also conclude that exchanges between these two disciplines will also be beneficial to our knowledge of the Homo sapiens brain. Documenting the anatomy among other human species and including the variation over time within our own species are approaches that offer us a new perspective through which to appreciate what really characterizes the brain of humanity today.
... Our understanding of the evolution of brain shape in the human lineage might be experiencing a reverse trend. Despite logical enthusiasm around early findings illustrating an exquisitely human brain shape and level of brain asymmetry (Holloway, 1981;Holloway and De La Coste-Lareymondie, 1982), it has been later noted that the typical brain shape in H. sapiens, which is characterized by a strong left-occipital rightfrontal asymmetry known as the Yakovlevian torque (Toga and Thompson, 2003) or occipital bending (LeMay, 1976;Holloway and De La Coste-Lareymondie, 1982;Chance and Crow, 2007;Balzeau et al., 2013), is present to a degree in both fossil human species and great apes (Gannon et al., 1998;Balzeau and Gilissen, 2010;Frayer et al., 2016;Neubauer et al., 2020). This casts doubt on the link between brain asymmetry and properly human cognitive abilities and still suggests that the evolution of human brain shape is best viewed as a gradual process toward exaggerated asymmetry and large size (Balzeau and Gilissen, 2010;Corballis, 2010;Gomez-Robles et al., 2013;Neubauer et al., 2018). ...
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Modern humans have larger and more globular brains when compared to other primates. Such anatomical features are further reflected in the possession of a moderately asymmetrical brain with the two hemispheres apparently rotated counterclockwise and slid anteroposteriorly on one another, in what is traditionally described as the Yakovlevian torque. Developmental disturbance in human brain asymmetry, or lack thereof, has been linked to several cognitive disorders including schizophrenia and depression. More importantly, the presence of the Yakovlevian torque is often advocated as the exterior manifestation of our unparalleled cognitive abilities. Consequently, studies of brain size and asymmetry in our own lineage indirectly address the question of what, and when, made us humans, trying to trace the emergence of brain asymmetry and expansion of cortical areas back in our Homo antecedents. Here, we tackle this same issue by studying the evolution of human brain size, shape, and asymmetry on a phylogenetic tree including 19 apes and Homo species, inclusive of our fellow ancestors. We found that a significant positive shift in the rate of brain shape evolution pertains to the clade including modern humans, Neanderthals, and Homo heidelbergensis. Although the Yakovlevian torque is well evident in these species and levels of brain asymmetry are correlated to changes in brain shape, further early Homo species possess the torque. Even though a strong allometric component is present in hominoid brain shape variability, this component seems unrelated to asymmetry and to the rate shift we recorded. These results suggest that changes in brain size and asymmetry were not the sole factors behind the fast evolution of brain shape in the most recent Homo species. The emergence of handedness and early manifestations of cultural modernity in the archeological record nicely coincide with the same three species sharing the largest and most rapidly evolving brains among all hominoids.
... Nevertheless, compared to modern humans from the same time period as them, Neanderthals have been found to be smaller in cranial capacity (unadjusted) at 200,000-76,000 years before present, and a match to them at 75,000-27,000 (Pearce et al., 2013), although it is not known whether these outcomes extend to cranial size overall. Temporal differences in cranial properties have been noted amongst modern humans, for instance, a fall in bizygomatic breadth and nasion-prosthion height when comparing modern humans of around 200,000-90,000 years before present to ones of the Holocene (Cieri et al., 2014), and cranial capacity was higher in late Pleistocene (25,000-92,000 years old) modern humans than in more contemporary ones (Balzeau et al., 2013). Results of research favour there having been a temporal fall in cranial capacity within the Holocene (e.g., Henneberg & Steyn, 1995). ...
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Gigantism and acromegaly have been observed in past populations; however, analyses usually focus on the morphological features of the post-cranial skeleton. The aim of this study is to characterize the internal anatomical features of the skull (brain endocast anatomy and asymmetry, frontal pneumatization, cranial thickness, sella turcica size) of an adult individual from the 11-14th centuries with these two diseases, in comparison with non-pathological individuals from the same population. The material consisted of 33 adult skulls from a mediaeval population, one of them belonging to an adult female with endocrine disorders (OL-23/77). Based on the CT scans, the internal cranial anatomy was analysed. The sella turcica of OL-23/77 is much larger than in the comparative sample. The endocast of the individual OL-23/77 shows a left frontal/left occipital petalia, while the comparative population mostly had right frontal/left occipital petalias. The asymmetry in petalia location in OL-23/77 comes within the range of variation observed in the comparative population. The individual has high values for cranial thickness. The frontal sinuses of the specimen analysed are similar in size and shape to the comparative sample only for data scaled to the skull length. Enlarged sella turcica is typical for individuals with acromegaly/gigantism. The pattern of the left frontal/left occipital petalia in the specimen OL-23/77 is quite rare. The position of the endocranial petalias has not influenced the degree of asymmetry in the specimen. Despite the large bone thickness values, skull of OL-23/77 does not show any abnormal features. The skull/endocast relationship in this individual shows some peculiarities in relation to its large size, while other internal anatomical features are within the normal range of variation of the comparative sample.
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Ultrasocial argues that rather than environmental destruction and extreme inequality being due to human nature, they are the result of the adoption of agriculture by our ancestors. Human economy has become an ultrasocial superorganism (similar to an ant or termite colony), with the requirements of superorganism taking precedence over the individuals within it. Human society is now an autonomous, highly integrated network of technologies, institutions, and belief systems dedicated to the expansion of economic production. Recognizing this allows a radically new interpretation of free market and neoliberal ideology which - far from advocating personal freedom - leads to sacrificing the well-being of individuals for the benefit of the global market. Ultrasocial is a fascinating exploration of what this means for the future direction of the humanity: can we forge a better, more egalitarian, and sustainable future by changing this socio-economic - and ultimately destructive - path? Gowdy explores how this might be achieved.
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We describe and evaluate the methods used to reconstruct the central nervous system (CNS) of extinct hominin taxa. Overviews of each hominin taxon are provided, focusing on evidence related to the evolution of the CNS. Trends in the evolution of the hominin CNS are investigated using these data. Encephalization in the hominin clade may have begun as early as Australopithecus afarensis and Au. africanus, but it is only with the appearance of Homo rudolfensis and H. habilis that both absolute and relative brain size have departed from a Pan-like condition. Brain size increase and the appearance of some aspects of modern humanlike brain morphology occur in at least two hominin lineages, Paranthropus and Homo, which have absolutely and relatively larger brains than Australopithecus. However, only fossil Homo taxa show a substantial increase in brain size and a shift to a modern humanlike brain morphology.
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Brain Endocasts is the only comprehensive, single-volume work dealing exclusively and uniformly with fossil hominid brain endocasts. Never-before-published photographs come together with easily accessible, coherent descriptions to create a detailed reference on the paleoneurological evidence for human evolution. Each entry offers essential information related to the location, dating, associations, and morphology of a given endocast. The text also covers the latest methodologies and techniques available for studying endocasts. In addition, a concise summary shows how these fossil records contribute to our understanding of human evolution and behavior.