bruner 2004

Journal of Human Evolution 47 (2004) 279e303

Geometric morphometrics and paleoneurology: brain shapeevolution in the genus Homo

Emiliano Bruner*

Dipartimento di Biologia Animale e dell’Uomo, Universita La Sapienza, P.le A. Moro 5, 00185 Roma, Italy

Istituto Italiano di Paleontologia Umana, P.za Mincio 2, 00198 Roma, Italia

Received 13 November 2003; accepted 18 March 2004

Abstract

Paleoneurology concerns the study and analysis of fossil endocasts. Together with cranial capacity and discreteanatomical features, shape can be analysed to consider the spatial relationships between structures and to investigate

the endocranial structural system. A sample of endocasts from fossil specimens of the genus Homo has been analysedusing traditional metrics and 2D geometric morphometrics based on lateral projections of endocranial shape. Themaximum and frontal widths show a size-related pattern of variation shared by all the taxa considered. Furthermore, as

cranial capacity increases in the non-modern morphotypes there is a general endocranial vertical stretching (mainlycentred at the anterior ascending circumvolution) with flattening and relative shortening of the parietal areas. Thispattern could have involved some structural stress between brain development and vault bones at the parietalmidsagittal profile in the heavy encephalised Neandertals. In contrast, modern humans show a species-specific

neomorphic hypertrophy of the parietal volumes, leading to a dorsal growth and ventral flexion (convolution) andconsequent globularity of the whole structure.

Brain tensors such as the falx cerebri have been hypothesised to represent one of the main physical constraints on

morphogenetic trajectories, with additional influences from cranial base structures. The neurofunctional inferencesdiscussed here stress the role of the parietal areas in the visuo-spatial coordination and integration, which can beinvolved in higher cerebral functions and related to conceptual thinking.

� 2004 Elsevier Ltd. All rights reserved.

Keywords: human evolution; endocranial morphology; fossil endocasts; brain shape

* Dipartimento di Biologia Animale e dell’Uomo, Universita La Sapienza, P.le A. Moro 5, 00185 Roma, Italy. Tel. C39 06 4991

2690; Fax: C39 06 4991 2771.

E-mail address: [email protected]

0047-2484/$ - see front matter � 2004 Elsevier Ltd. All rights reserved.

doi:10.1016/j.jhevol.2004.03.009

mailto:[email protected]

280 E. Bruner / Journal of Human Evolution 47 (2004) 279e303

Introduction

Considering the tight ontogenetic relationshipbetween brain shape and skull bones (Moss andYoung, 1960; Enlow, 1990), the endocasts fromfossil crania are a useful source of information onhominid cerebral morphology and anatomy. Thisprinciple is the basis of paleoneurology, namelythe examination and analysis of natural orartificial endocasts that reproduce details of theexternal morphology of the brain (Holloway,1978; Falk, 1986, 1987; Bruner, 2003a).

Although brain size has been the principal issueconsidered in the paleoanthropological literature,paleoneurology also focuses on specific anatomicaltraits, like vascular patterns (e.g. Kimbel, 1984;Falk, 1993; Saban, 1995; Grimaud-Herve, 1997),cerebral asymmetries (Le May, 1976; Hollowayand De La CosteLareymondie, 1982), or specificcircumvolutions (Grimaud-Herve, 1997).

Brain shape variation has rarely been analysed,mainly because of the fragmentary nature of thefossil record. Furthermore, there are some diffi-culties in coding and quantifying endocranialmorphology, because of the smooth geometry ofthe brain itself. A pioneering approach to endo-cranial shape variation in fossil hominids wasperformed using a polar coordinate stereoplottingtechnique to compare extant and extinct Homi-noidea (Holloway, 1978, 1981a). This researchsuggested that a large amount of variation can belocalised in the lower parietal areas in the extanttaxa, and in the upper parietal districts consideringthe extinct groups.

It has been hypothesised that early changes inthe frontal areas in Australopithecus were followedby a late and gradual evolution of posteriordistricts in early human representatives (Falket al., 2000). In earlier hominids the principaldifferences from apes may have been a reductionof the primary visual striate cortex, a reorganisa-tion of the frontal lobe (mostly at the third frontalcircumvolutions), and the expression of hemi-spheric specialisation (Holloway, 1995). Subse-quently, the development of the posterior parietalcortex may have been related to an increase invisuospatial integration, sensory reception, andsocial communication.

One of the most studied area in fossil endocastsis represented by the frontal lobes, because of theirpresumed role in higher cognitive functions andlanguage. Generally, the frontal lobes are nar-rower in the most archaic Homo taxa, showinga clear ‘‘encephalic rostrum’’ (Grimaud-Herve,1997). The lateral development of these structuresin more encephalised hominids leads to a morepronounced expression of the Broca’s cap, whichis involved in speech potentialities (e.g. Aboitizand Garcia, 1997; Cantalupo and Hopkins, 2001).The frontal midsagittal profile is less variable,without marked shape differences between MiddlePleistocene and modern humans (Bookstein et al.,1999). The position of the frontal lobes can bestrongly influenced by a marked pneumatisation,which pushes backward the entire orbital plate insome robust Middle Pleistocene specimens such asPetralona and Kabwe (Seidler et al., 1997). At theopposite extreme, the occipital lobes project back-ward behind the parietal profile in more archaicbrains, shifting under the parietal areas as brainsize increases. Accordingly, the cerebellar struc-tures are located under the occipital poles inarchaic Homo erectus, under the parietals in morederived taxa and almost under the temporal areasin modern humans (Grimaud-Herve, 1997). Thebrain’s maximum width is located at the temporalbase inHomo erectus and other Middle Pleistocenegroups, between the temporal and parietal areas inNeandertals, and at the parietals in anatomicallymodern humans (Holloway, 1980; Grimaud-Herve, 1997; Seidler et al., 1997). KNM-WT15000 (dated to about 1.5 Ma) and the otherspecimens included in the Homo ergaster hypo-digm show an endocast comparable to those ofAsian Homo erectus, but with a less developedfrontal diameter and without a marked occipitalprojection (Begun and Walker, 1993).

A recent study on the shape variation of theendocast in the genus Homo showed two majorpatterns of variation (Bruner et al., 2003): anarchaic structural trajectory shared by non-modern taxa and characterised by an allometricvertical development, frontal enlargement, andparietal relative shortening, versus a modern pat-tern characterised by parietal development leadingto brain globularity.

281E. Bruner / Journal of Human Evolution 47 (2004) 279e303

In this paper, the endocranial shape of somefossil specimens included in the hypodigm of thegenus Homo is investigated using traditionalmetric comparisons and two-dimensional geomet-ric morphometrics performed on projected lateralviews of the endocast. The aim is to consider indetail some specific variables of the human fossilendocasts, and to characterise the endocranialmorphology in norma lateralis. This approach isused to check and improve previous results fromthree-dimensional analyses. The lateral view (andparticularly the midsagittal vault profile) has beenfrequently considered in evolutionary studiesbecause of its recognised availability, usefulness,and evolutionary meaning (e.g. Manzi et al.,2000b; Lieberman et al., 2002; Bruner et al.,2004). Also, projections and 2D data allow theuse of type III landmarks (Bookstein, 1991),geometrically defined by chords or fractions ofcurvature. Type III landmarks have no biologicalmeaning in terms of homology, but can be used todefine structures or areas that lack clear anatom-ical references. These points can be extremelyuseful when considering endocranial shape, forwhich type I (i.e. homologous) and type II(structurally corresponding) landmarks are rare.

The null hypothesis of this analysis is thathuman brain evolution was based on quantitativeencephalisation, i.e., endocranial enlargementwithout change of the structural model. Thishypothesis suggests that endocranial variationwithin the genus Homo was characterised byscaled (i.e. allometric) versions of a plesiomorphicmorphological plan, described by a shared struc-tural trajectory. Conversely, the recognition ofgroup-specific patterns would suggest the presenceof neomorphic processes.

Materials and methods

Comparative samples

Data were collected from high-quality endo-casts at the Museum of Anthropology ‘‘GiuseppeSergi’’ (Dipartimento di Biologia Animale edell’Uomo, Universita La Sapienza, Roma), theIstituto Italiano di Paleontologia Umana (IsIPU,

Roma), and the Institut de Paleontologie Humaine(IPH, Paris).

As in previous analyses (Bruner, 2003b; Bruneret al., 2003), the specimens were included inthree main groups in order to identify generalpatterns:

1. Archaic morphotypes (ARC): specimens re-ferred to Homo erectus sensu lato (s.l.), namely theAsian Early and Middle Pleistocene remains(Homo erectus sensu stricto e s.s.) plus thespecimens from Sale (Africa) and Arago (Europe).It is assumed that, even if the Asian specimensshow some apomorphic or autapomorphic traits,they represent a less derived model with respect toNeandertals and modern humans. The Sale skull isnot entirely interpreted, but it is assumed torepresent a plesiomorphic pattern compared tomore encephalised taxa of the genus Homo.Asymmetries at the nuchal ectocranial structurein Sale suggest a pathological congenital torticollis,related to atrophy of some nuchal muscles, andasymmetrical reduction of the surface insertions(see Hublin, 2002). In contrast, no markedasymmetry is shown at the internal surface, exceptfor minor differences related to a common leftoccipital petalia tilting the midsagittal axis and theunderlying cerebellar poles. Furthermore, therelative independence between inner and outertables of the skull (involving epigenetic muscle-related traits) suggests that endocranial morphol-ogy is not strongly affected by the hypothesisedectocranial pathology.

The Arago endocast is the result of a hybridreconstruction composed of the Arago frontal andparietal (respectively Arago 21 and Arago 47) andthe occipital from Swanscombe and the temporalsfrom Sangiran 17. Therefore, it represents a het-erogeneous but in any case less derived systemwith respect to Neandertals and modern humans.Clearly, all of these assumptions are based on a setof inferences about the phylogenetic status of thesespecimens, but they are necessary to producea reference variability

2. Neandertals (NDR): European WurmianNeandertals, here recognised as Homo neandertha-lensis. A stereolithographic model of the virtualendocast of Saccopastore 1 (Bruner et al., 2002)has been included in this group. Although the


fossils from Saccopastore are dated to about 120Ka, they show Neandertal derived traits both forthe ectocranial (Sergi, 1944; Condemi, 1992) andendocranial (Bruner, 2003b) morphology. Theskull from Teshik-Tash represents a juvenile in-dividual, but its ontogenetic stage is assumed notto affect the endocranial comparison. Braingrowth is almost complete at this age, with thebrain weight of modern human populations rea-ching 96% and 99.7% of the adult values atthe puberty and adolescence respectively (Pena-Melian, 2000). Furthermore, Neandertal cranialshape shows rate-hypermorphosis compared tomodern humans, and the taxonomic differencesare expressed early during ontogeny (Ponce deLeon and Zollikofer, 2001). According to itscranial development, Teshik-Tash, about 8.5 yearsold, is comparable to Qafzeh 11, approximately13.5 years old (Ponce de Leon and Zollikofer,2001). Therefore, the cranial shape must beassumed sufficiently comparable with the adultspecimens.

3. Modern Humans (MOD): anatomically mod-ern humans, from Late Pleistocene to recentpopulations. This group includes the endocast ofVatte di Zambana, recovered near Trento (Italy) in1967-68 and dated to 8 ka (Corrain et al., 1976;Newell et al., 1979). A modern endocast froma recent Javan individual is also included in thisgroup. It shows an extreme brachycephalic ex-pression of the modern cerebral packing, present-ing an almost globular structure that may be usefulto understand the trends and variability of theHomo sapiens model.

In Table 1 a list of the entire sample is provided,with information about the repository source, thereference group, and the labels used in the text.

Univariate and bivariate metrics

Fig. 1a shows the diameters employed in thisanalysis, and Table 2 provides a list of theendocranial variables, together with the respectivelabels and definitions. Lengths and widths weremeasured with a spreading caliper directly on theendocast. Chords and heights were measured byprojecting the respective landmarks onto the lefthemisphere in lateral view through a dioptograph.

Endocasts were aligned using the plane passingthrough the frontal crest, the internal occipitalprotuberance, and the endovertex. Absolute valueshave been considered as well as relative values,which were divided by the maximum length of theendocast (averaged hemispheres). Differences be-tween groups were analysed by Kruskal-Wallisanalysis of variance. Regressions were analysed bythe least-squares procedure and both Pearson’sand Spearman’s correlation coefficient. Statisticalsignificance was set at p ! 0.05. A Major Axisregression has been computed by Model II(Legendre, 2001 - http://www.fas.umontreal.ca/biol/legendre). Repeated measures of diameterson the endocast sample revealed an average errorof 0.6 mm, due mostly to uncertainty in local-isation of type II (Bookstein, 1991) and fuzzylandmarks (Valeri et al., 1998). The maximumaverage error for repeated measures was 0.9 mm (adiscrepancy less than 5%). Considering theselimits in the metric resolution, the diameters weretaken to the nearest millimetre.

Table 1

List of the whole sample, with labels used in the text, reference

group, and repository site

Specimen Label Group Repository*

Trinil 2 TRN2 ARC IsIPU

Sangiran 2 SNG2 ARC IPH

Sale SAL ARC BAU

Sinanthropus III ZKD3 ARC BAU

Sinanthropus X ZKD10 ARC IPH

Sinanthropus XII ZKD12 ARC IsIPU

Arago (rec) ARA ARC IsIPU

Saccopastore 1 SCP1 NDR BAU

La Chapelle-aux-Saints CHP NDR IsIPU

La Ferrassie 1 FRS NDR IPH

Teshik-Tash TST NDR IPH

Guattari 1 GTT NDR IsIPU

Feldhofer Grotto FLD NDR BAU

Predmostı 3 PRD3 MOD IPH




Combe-Capelle CCP MOD IsIPU

Vestonice 2 VST2 MOD IPH

Vatte di Zambana VTT MOD IsIPU

Recent Human Endocast RHE MOD IPH

*BAU: Dipartimento di Biologia Animale e dell’Uomo.

IsIPU: Istituto Italiano di Paleontologia Umana.

IPH: Institut de Paleontologie Humaine.

http://www.fas.umontreal.ca/biol/legendre

http://www.fas.umontreal.ca/biol/legendre


Fig. 1. a) Interlandmark distances sampled on the endocasts, in left lateral and upper view. The diameters have been measured directly

on the endocasts, while chords and projections have been obtained using a dioptograph (see Table 2 for labels and definitions). b)

landmark configuration used in the 2D geometric morphometric analysis (left hemisphere - see Table 3 for labels and definitions); for

the PCA a reduced configuration has been used, considering only the vault morphology (landmarks between FP and OP).

Geometric morphometrics

Endocranial shape was also analysed by a land-mark-based approach, according to the proce-dures of geometric morphometrics (Bookstein,1989; Rohlf and Bookstein, 1990; Bookstein,1991; Marcus et al., 1993; Rohlf and Marcus,1993; Marcus et al., 1996). In geometric morpho-metrics, systems of coordinates are superimposedto minimise the size differences between specimens,with the aim of identifying the shape component ofthe total form (see Richtsmeier et al., 2002; Rohlf,2003). A two-dimensional configuration of nine-teen landmarks was selected to describe theendocranial lateral profile. Landmarks were cho-sen based on an operational homology definition(see Smith, 1990). Table 3 shows the list oflandmarks, together with their labels and defini-

tions. Fig. 1b shows the entire configuration. Theleft hemisphere was used, except for CombeCapelle that shows excessive damage on that side.A Generalised Procrustes Analysis (GPA) wasperformed, except in the 2D pairwise comparisonin which a Bookstein superimposition was pre-ferred. The first procedure superimposes theconfigurations through translation of the cent-roids, scaling to unitary size, and least-squarerotation, while the second uses a reference baselinebetween two landmarks (Bookstein, 1991). For theBookstein superimpositon the frontal and occipitalpoles were used as references for the baseline. Thissuperimposition was used in the pairwise compar-isons considering the hemispheric length a goodindex of quantitative encephalisation, useful todisplay differences in shape at the same endocra-nial antero-posterior development. Furthermore,


Table 2

List of the interlandmark distances used in the metric analysis, with labels and definitions

Label Measure Definition

ML maximum length maximum hemispheric length from frontal to

occipital poles - averaged hemispheres

MW maximum width maximum width of the endocast, orthogonal to

the midsagittal cerebral plane

BW Broca width maximum width of the endocast at the base of the third

frontal circumvolution

H1 anterior height vault height at the anterior quarter - 25% - of the maximum

length chord

H2 middle height vault height at the middle - 50% - of the maximum

length chord

H3 posterior height vault height at the posterior quarter - 75% - of the

maximum length chord

VM vault module mean value between maximum length, maximum

width and middle height

FC frontal chord chord between the most anterior point of the frontal pole and the

rolandic scissure at the midsagittal plane

PC parietal chord chord between the Rolandic scissure and the perpendicular

scissure at the midsagittal plane

OC occipital chord chord between the perpendicular scissure and the torcular

herophili at the midsagittal plane

this configuration is mainly based on the anteriorand posterior extremes. Anyway, in this analysissuperimpositions using the baseline or the pro-crustes procedure gave the same results, moreevidenced in the former approach. Centroid size isused as size index, defined as the square root of thesum of squared distances of a set of landmarksfrom their centroid (Marcus et al., 1996). Datawere sampled using a dioptograph and digitised bytpsDig 1.20 (Rohlf, 1998a). The Principal Compo-nent Analysis (PCA) required a minimum statis-tical balance between specimens and landmarks,and the use of missing data was unsuitable.Therefore, to keep a sufficient fossil sample, onlythe landmarks from the vault (between FP andOP) were used (9 landmarks, 21 specimens). Thevault configuration was used in a Cluster Analysisof individual specimens based on the Procrustesdistance matrix and the unweighted pair-groupmethod using arithmetic averages (UPGMA). Asstressed before, this analysis is aimed at character-ising phenotypes only in terms of shape, havinglandmarks a geometrical and structural meaning.

The perpendicular scissure (i.e. the crossingpoint in lateral view between this scissure and theinterhemispheric one) has not been used in the 2D

configuration because of incompatibility betweenfixed homologous landmarks and shifting geo-metric landmarks. The sequence along the midlinepresents the perpendicular scissure situated be-tween the 2nd and 3rd posterior chord projection(thus, between P2 and P3) in Homo erectus andHomo sapiens specimens. In contrast, in Nean-dertals and the specimen from Sale the perpendic-ular scissure lies before the midpoint of theposterior projection (thus, anterior to P2). This isprobably related to the occipital projection inHomo erectus, and to the parietal development inHomo sapiens. This inversion leads to somevisualisation difficulties in spatial deformation,but it is still a useful geometric indication thatmust be considered in future studies. Consideringthe landmarks used in these analyses, it must bestated that the terms ‘‘parietal’’ is used here todescribe a surface that should overlap with theunderlying cortical structure. When the Rolandicand perpendicular scissures are involved (as in theinterlandmark metrics), this relationship is quitetight, and it is used to describe the presumedboundaries of the parietal lobes. Conversely, whenthe general outlines are considered (as in thegeometric morphometric approach), ‘‘parietal


Table 3

List of the landmark used in the geometric morphometric analysis, with labels and definitions

Label Landmarks Definition

FP frontal pole the most anterior point of the endocast according to the maximum length

RS rolandic scissure meeting point between the rolandic and interhemispheric scissures

F1-F3 frontal projections meeting points between the endocranial outline and orthogonal chords drawn

at fractions of the frontal chord (respectively at 0.25, 0.50, 0.75)

OP occipital pole the most posterior point of the endocast according to the maximum length

P1-P3 posterior projections meeting points between the endocranial outline and orthogonal chords

drawn at fractions of the posterior chord (respectively at 0.25, 0.50, 0.75)

TH torcular herophili point of maximum depression at the internal occipital protuberance

TOC temporo-occipito-cerebellar meeting point between the cerebro-cerebellar scissure and the preoccipital

scissure, between the 3rd temporal and 3rd occipital circumvolutions

TV temporal valley posterior end of the temporal valley, between the temporal and cerebellar areas,

at the angle between the temporal and cerebellar lobes

ACC anterior cerebellar anterior point of the cerebellar outline, at the meeting

with the temporal lobe

PCC posterior cerebellar posterior point of the cerebellar outline, at the meeting

with the occipital lobe

C1-C3 cerebellar projections meeting points between the cerebellar outline and orthogonal chords drawn at

fractions of the cerebellar chord ACC-PCC (respectively at 0.25, 0.50, 0.75)

TP temporal pole point of maximum curvature of the temporal lobe

BA Broca area point of maximum curvature between the pars opercularis and pars

triangularis at the 3rd frontal circumvolutions

areas’’ are used to describe surfaces that are notnecessarily related to specific circumvolutions.

Other functionally interesting structures - likethe supramarginal gyrus or other specific circum-volutions - have not been included in this analysisbecause of the excessive uncertainty with respect tothe available variation. For the supramarginalgyrus, problems arose in the exact localisation ofthe boundaries of this area, which is smooth andirregular. This gyrus is included in Wernicke’s areaand it represents one of the major sources ofasymmetry in the human brain, generally beingmore strongly expressed on the left hemisphere.Therefore, cerebral dominance leads to a differentlocation of the homologous counterpart on theright side. Once the gyrus has been localised, thechoice of the landmarks to represent this area isnot unequivocal, and often the centroid of the bossdoes not overlap with the point of maximumcurvature of the circumvolutions. Structures likethe supramarginal or the angular gyrus would bebetter considered only in group-averaged andhemisphere-averaged data.

As cautionary note, it must be noted thebidimensional projections of volumes can be

misleading if the geometric properties of the modelare not considered carefully. In this 2D configu-ration, the results will be influenced by thedifferent orientation of specific areas, as thecerebellar lobes. The more angled they are relativeto the midsagittal plane, the shorter they willappear to be in a 2D projection. In any case, suchan approach is necessary to consider geometricallyderived landmarks from chords and projectionsand to characterise areas that lack clearly local-isable points. It must be stressed that, because ofthe group-specific limited sample size, it is difficultto conduct between-group tests of significance.Instead, pairwise comparisons, cluster procedures,and multivariate approaches are used to character-ise and describe the main phenotypic affinitiesamong specimens. Morpheus et al. (Slice, 2000 -http://life.bio.sunysb.edu/morph/) was used tocompute average shapes and pairwise compari-sons. Applied Procrustes Software 2.3 (APS; Penin,2000 - http://www.cpod.com/monoweb/aps/) andtpsRelw 1.18 (Rohlf, 1998b - http://life.bio.sunysb.edu/morph/) were used for the PCA. Procrustesdistances were obtained by tpsSmall 1.19 (Rohlf,1998c). Cluster Analysis was performed by

http://life.bio.sunysb.edu/morph/

http://www.cpod.com/monoweb/aps/




UPGMA using the Phylogeny InferencePackage (PHYLIP, 3.57c; Felsenstein, 1989- http://evolution.genetics.washington.edu/phylip.html), while phenograms were computed withTREEVIEW (Page, 1996 - http://taxonomy.zoology.gla.ac.uk/rod/treeview.html).

Results

Univariate and bivariate metrics

Univariate distributions are reported for eachmain group by median and quartile values (Table4). Considering the absolute diameters, the morederived groups (NDR and MOD) show signifi-cantly larger values for the vault module andmaximum endocranial length when compared tothe archaic average.

Neandertals and modern humans show a signif-icant larger value for the frontal chord, withmodern humans also showing a larger parietalchord. Considering the relative values, Neandertalsdisplay a larger frontal and a shorter parietal chord,while modern humans have a relatively greaterdevelopment of the parietal value. A bivariate plotof frontal and parietal chords shows that, movingfrom the archaic specimens (mostly the smallindividuals) to the Neandertals, an increase of thefirst value is not associated with an increase of thesecond. In contrast, the modern sample shows anincrease in both variables (Fig. 2a).

The vault heights show a clear pattern ofincreasing values from the archaic group toNeandertals to modern humans. The differencesbetween NDR and MOD are significant for theposterior height (H3 - both absolute and relativevalues). The anterior and middle heights showsignificant differences for the smaller values of thearchaic group (absolute data) or between archaicand modern humans (relative data), even if thetrend is similar to that of posterior height. Theheights show the strongest correlation withthe vault module (r Z 0.87, 0.91, and 0.85respectively). Considering this allometric relation-ship, the modern specimens seem to depart froma trajectory shared by the non-modern sample(Fig. 2b). The differences in the relative height
T
able

4

Medianandquartiles

forabsolute

andrelativemetrics

inthethreegroups(absolute

values

are

inmm)

ML

FC

PC

OC

MW

BW

H1

H2

H3

VM

BW/M

WFCr

PCr

OCr

H1r

H2r

H3r

MWr

BWr

ARC

med

158

102

53

60

126

92

50

59

52

112

0.74

0.66

0.31

0.37

0.30

0.36

0.31

0.77

0.58

25(

149

101

49

55

119

85

47

55

47

108

0.71

0.65

0.31

0.35

0.30

0.36

0.30

0.75

0.57

75(

172

114

55

65

129

96

52

63

55

121

0.76

0.68

0.36

0.39

0.31

0.38

0.33

0.81

0.58

NDR

med

175

124

46

70

140

111

57

68

56

129

0.78

0.71

0.26

0.38

0.33

0.39

0.33

0.80

0.62

25(

173

119

44

62

138

108

55

67

55

126

0.78

0.69

0.25

0.38

0.31

0.37

0.32

0.79

0.62

75(

183

129

47

70

145

113

61

75

64

133

0.79

0.73

0.27

0.40

0.34

0.41

0.36

0.82

0.64

MOD

med

184

122

78

70

139

110

66

79

71

133

0.80

0.67

0.43

0.38

0.38

0.45

0.40

0.76

0.62

25(

177

117

74

63

136

103

61

76

69

131

0.75

0.64

0.40

0.36

0.33

0.40

0.37

0.75

0.57

75(

188

123

84

73

142

114

69

83

75

136

0.82

0.68

0.47

0.39

0.39

0.46

0.42

0.77

0.63

http://evolution.genetics.washington.edu/phylip.html

http://evolution.genetics.washington.edu/phylip.html

http://taxonomy.zoology.gla.ac.uk/rod/treeview.html

http://taxonomy.zoology.gla.ac.uk/rod/treeview.html


Fig. 2. Bivariate comparisons. a) frontal chord vs. parietal chord. b) vault module vs. posterior height (H3). c) slopes (alpha) for the

regression between vault module and heights (H1, H2, H3) for the non-modern (bold line) and modern (plain line) groups. d)

maximum width vs. frontal width at the Broca’s cap. The three groups are represented by circles (ARC), squares (NDR) and triangles

(MOD). Values are in mm. See Table 1 for labels.

values are attenuated but confirm the gradualincrease between the main groups, and for theposterior height the differences are again pro-nounced. A full statistical approach to the species-specific regression coefficients has not beenperformed because of the limited sample size.Nevertheless, if we pool the archaic and Neander-tal specimens into a non-modern group, theregressions between vault module and heightsshow a set of slopes distinctly different from themodern pattern (Fig. 2c). Interestingly, the within-group scheme seems comparable (with middleheight more sensitive to size), but with highervalues in the modern group. Among the relative

measures, heights are the only variables maintain-ing a significant correlation with the vault module(r Z 0.48, 0.58, and 0.58 respectively).

The maximum width presents significantlygreater values for moderns and Neandertals,slightly higher for the latter group. When themaximum width is corrected for the hemisphericlength, the differences seem to fade, with a largerange of variation in modern humans and slightlyhigher mean values for Neandertals. The modernrange is strongly influenced by the rounded (wideand short) RHE endocast and the lengthened (thinand long) VST2 brain. The width at Broca’s capshows an absolute distribution very similar to the


maximum width. With respect to the hemisphericlength, the mean values of the two derivedmorphotypes are still above that of the archaicgroup. The ratio between the Broca and maximumwidths expresses an archaic pattern, with a limitedfrontal diameter compared with the total breadth,and two derived morphotypes (Neandertals andmoderns) with relatively enlarged frontal width. AKruskal-Wallis test between archaic and non-archaic values is significant at 0.08 level (which isindicative, considering the small number of speci-mens). A bivariate plot of MW vs. BW (Fig. 2d)suggests no clear species-specific departure froma shared trajectory. A correlation between thesetwo diameters and the vault module showscoefficients of 0.84 (MW) and 0.91 (BW). In-terestingly, a least square regression shows thefrontal width scaling with a slope of 0.95, while themaximum (parieto-temporal) width scaling witha slope of 0.80. Because of the small sample size,the 95% confidence intervals of these slopes arelarge, overlapping each other and both includingisometry. The major axis computed on the samevariables shows slopes respectively of 0.94 (maxi-mumwidth vs. vault module) and 1.04 (Broca widthvs. vault module), with the same considerations onthe confidence intervals. In general, this secondapproach would be more appropriate to analyse therelationship between two variables but, because ofthe limited sample size and because of the likelynon-normal distribution of the variation (whichincludes multiple taxa), it could be a less robustresult (seeMartin and Barbour, 1989; Legendre andLegendre, 1998). The regressions are all significant,but the coefficients cannot be properly analysed andshould be considered only indicative. Generally,these data may suggest that as size increases thefrontal diameter widens slightly faster than themaximum (temporo-parietal) breadth.

The occipital chord is larger in Neandertals andmodern humans, but the differences are notsignificant when the relative values are considered.

Geometric morphometrics

The PCA applied to the vault coordinatesshows a polarised morphospace, in which the firsttwo components account for 89% of the total

variance (Fig. 3a). The 1st component (69% of thetotal variance) is related to parietal development.At lower values the parietal outline flattens andshortens, with consequent relative lengthening ofthe vault. The frontal area enlarges and bendsupward, while the occipital pole undergoes a ver-tical shortening. At higher values, the parietal areagrows almost orthogonal to the midsagittal profile.The vault thus becomes higher and relativelyshorter, with reduction of the most frontal surfaceand vertical development of the posterior districts.

This first axis mostly separates modern humans,with a developed parietal outline and shortenedfrontal and occipital poles, from non-modernspecimens, which show endocranial flattening atthe parietal outline. The 2nd component (20% ofthe total variance) involves a general stretching ofthe vault vertically at lower values and a verticalflattening on at higher values. The verticalstretching/flattening is particularly localised ante-rior to the Rolandic scissure, namely at theascending frontal circumvolutions. This secondaxis separates Neandertals with relatively highvaults and developed frontal areas, from thearchaic samples, which are more platycephalicand have a reduced frontal development. Themodern sample is split by this component intomore rounded profiles versus high and lengthenedones (mostly VST2 and CCP). A plot of the firsttwo principal components shows a good separa-tion of the three main groups (Fig. 3b), modernhumans showing a developed parietal outline,Neandertals displaying high vaults and flattenedparietals, and the archaic group with a low vaultand flattened parietals. The following axes arerelated to small percentages of variability (!4%).When the first axis is plotted against the centroidsize, two clusters are easily identified (Fig. 3c). Themodern sample is separate, with large size andderived parietal growth. The other two groups liecontiguously with Neandertals having larger butslightly more flattened parietals. Therefore, in non-modern specimens there is a change of size withoutmarked changes of shape, while there is a morpho-logical gap between modern and non-modernspecimens in the relationship of shape to size.Considering the whole shape variation, bothmultiple regression and partial least-square


Fig. 3. Vault shape 2D analysis. a) distortion grids showing the two extreme configurations along the PC1 and PC2 vectors (left

hemisphere). PC1 is mainly characterised by parietal reduction/development, with consequent bending/convolution of the vault. PC2

describes a vertical stretching/flattening of the vault, localised mainly anteriorly to the Rolandic scissure (frontal ascending

circumvolution) b) plotting of PC1 and PC2 values computed on the Procrustes residuals. c) PC1 values are plotted against centroid

size (groups and labels like Fig. 2).

regression onto centroid size do not find otherallometric vectors. Considering just the archaicand Neandertal specimens, a PCA shows a firstaxis of variation weakly correlated with centroidsize (partial least-square regression: r Z 0.64,p Z 0.02), separating archaic specimens fromNeandertals, and involving (from smaller tolarger configurations) parietal flattening andshortening associated with frontal vertical de-velopment (Fig. 4). Clearly, a larger number ofspecimens would be required for a useful statis-tical approach to the species-specific allometricpattern.

A UPGMA applied to the Procrustes distancesbetween specimens using this endocranial vaultconfiguration shows the main separation to bebetween modern and non-modern samples(Fig. 5a). Within the non-modern group, Archaicand Neandertal specimens show two principalclusters that, however, do not represent exactly thetwo respective taxa. The Asian Homo erectusspecimens show a close phenetic affinity to eachother.

Using the complete configuration, the consen-sus average shapes of the two more derived groupswere compared to the mean archaic configuration


by superimposition of the fronto-occipital baseline(Fig. 5b).

ARC vs. NDR. The entire structure stretchesvertically in NDR, and the frontal area enlarges.The occipito-cerebellar complex shifts forward.There is increased development of the temporo-occipital surface. The grid generally describes avertical development, with an upward bending ofthe vault. The endocast undergoes a slight dorsalflexion by means of an upward shifting of the ex-tremities and a retrograde movement of the upperlandmarks. The internal occipital protuberance(and the whole posterior district) shows a geomet-ric compression, as a structural meeting point offorces deriving from the dorsal bending and verti-cal stretching. The confluence of sinuses becomesless deepened under the flattening occipital poles.

ARC vs. MOD. The vault enlarges and developsvertically in MOD, mostly because of anextreme enlargement of the parietal contour. Thevault development involves an opposite bendingwith respect to the previous pattern, namely a‘‘convolution’’ of the whole structure. The term‘‘convolution’’ is used here not to describe anincrease of the cerebral gyrification, but to describea dorsal (parietal) growth that involves a globular-isation process of the entire structure. While theparietal enlarges, the temporo-cerebellar areasapproach the frontal poles. The extremities turndownward by the action of the parietal pressure,approaching each other with shortening of the

Fig. 4. PC1 values from a PCA including only the non-modern

specimens (ARCCNDR). The grids show the relative distor-

tion in the two opposite directions of the morphological vector.

basal lengths and the development of a morerounded morphology. The relative endocraniallength decreases, with relative shortening of thefrontal and occipital poles. The cerebellum ispushed downward by this deformation.

A further note can be added regarding theposition of the Rolandic scissure. Generally, innon-modern specimens the Rolandic scissure liesbehind the midpoint of the maximum length, andthe middle vault height (H2) crosses the profileapproximately at the frontal ascending circumvo-lution. In contrast, in modern humans the middleheight position approaches the Rolandic scissure,or even lies behind it, at the ascending parietalcircumvolution.

Discussion

Methodological considerations

Paleoneurology generally has limitations be-cause of the poor preservation of fossils, the lowprevalence of brain traces on the inner table, a verysmall sample size, and the heterogeneous trainingof the few scholars working on this issue (Hollo-way, 1978). Metric tools in paleoneurology presentseveral additional challenges.

First, cerebral landmarks are seldom clearlylocalisable, because of the ‘‘fuzzy’’ nature of thewhole structure. ‘‘Fuzzy landmarks’’ have beendefined as ‘‘the position of a biological structurethat is precisely delineated, but occupies an areathat is larger than a single point in the observer’sreference system’’ (Valeri et al., 1998). However,a within-observer error test proved that theuncertainty of fuzzy landmarks is limited and canbe reduced by experience; moreover, literaturestudies report errors comparable with the valuesreported in this analysis for the more localisablelandmarks (Valeri et al., 1998; Free et al., 2001).

Type I landmarks (biologically homologous)are rare, and most of the suitable references can beincluded in type II, such as points of maximumcurvature, projections or depths. Many of theendocranial landmarks are often ‘‘hard Type II’’,i.e. defined by smooth surfaces or strongly de-pendent on variables like the orientation of the


Fig. 5. a) UPGMA phenogram computed on the Procrustes distance matrix from the geometric morphometric analysis of the vault; b)

distortion grids showing the pair-wise comparison between averaged configurations after Bookstein superimposition (baseline: FP-

OP): ARC compared to MOD (top), and ARC compared to NDR (bottom). Reference shape (ARC) in bold.

specimen or even the handling of the surfaces.Actually, both orientation and perspective playa crucial role during the localisation of somepoints. For the same reasons, there are few andweak references available to build geometricconstructed landmarks, such as chords or projec-tions. Asymmetries play an additional confound-ing role, making landmarks and diametersextremely dependent upon hemispheres and lead-ing to easy misinterpretation of morphologicalrelationships. One of the consequences of hemi-spheric asymmetry is the curvature of the in-terhemispheric scissure, which is the only referenceavailable to localise the midsagittal plane. There-fore, the only plane available to localise landmarksand relative diameters is rather biased by the director indirect influence of cerebral dominance.

Incompleteness of specimens, damage, subjec-tivity of the reconstructions, and limits of mould-ing techniques must be taken into account withinthis context. Thus, a constant ‘‘anatomical un-certainty’’ will necessarily be involved in any dataset, and any inference will necessarily be limited bysome sort of morphological doubt. Even the raretype I landmarks are not immune from subjective

decisions. Points such as the Rolandic or thetransverse scissure at the midsagittal plane areseldom easily recognised on an endocast, anda certain degree of experience and ‘‘personalintuition’’ is required. Moreover, they representthe boundaries of some circumvolutions, andtherefore are often expressed not as points but asareas, whose geometry shows a high inter-individual variation. Experience can limit randomerror (within-observer), but the results may beinfluenced by a certain degree of systematicdiscrepancy (among-observer).

Two more sources of biases must be considered.First, the correspondence between endocranial andbrain morphology is not complete and univocal,and the endocasts represent only a part of thecerebral structures (Mannu, 1911; Kimbel, 1984;Zollikofer and Ponce de Leon, 2000). Second,cranial capacity and brain size do not overlapentirely, as cranial capacity includes a subarach-noidal space of about 300 cc (see Pena-Melian,2000). These biases are obviously related, with thesecond being the main cause of the first. Therefore,much caution has to be used when inferencesabout brain morphology are made from endocast


analyses, which mainly describe the variation ofendocranial features and not the original cerebralstructures. All the noise generated by thesevariables affects the resolution power of thepaleoneurological approach, as well as any land-mark-based analysis on cerebral living tissues(Free et al., 2001). The control and considerationof these properties represent the operational basesof paleoneurology. Data must be calibrated on theresolution power available, and results must bediscussed only on the basis of a robust approach,taking into account the real numeric meaning ofphysical differences. It must be remarked that themethodological notes described in this contextshould be considered not as limits of the approach,but as a priori parameters of the models used inthis analysis. They represents limits when ignored,confounding and producing noise in the results. Incontrast, they become intrinsic components of themodel if taken into account, improving the rangeof available analysis. Clearly, a more completeand resolute formalisation of brain geometrymust be one of the main future targets of paleon-eurologists.

In this paper, univariate and bivariate metricsand 2D geometric morphometrics generally sup-port and improve the results obtained froma multivariate interlandmark approach and 3Danalyses (Bruner et al., 2003). A comparisonbetween the two studies is useful to reinforce theresults considering the possible biases of thepaleoneurological approach. The data from 3Danalysis of the endocasts are largely based on typeI landmarks, related to a specific biologicalmeaning, but more scattered on the surface andassociated with a larger uncertainty related to theexact localisation of the structures (e.g. theperpendicular scissure). In contrast, the presentanalysis is based largely on type III landmarks,and a lateral projected bidimensional geometry.Thus, information is not associated with specificfunctions but simply with overall shape andmorphology. Furthermore, in the present paperthe complementary metrics from interlandmarkdistances strengthen the results because theycontribute to a synthetic approach, includinginformation from the third dimension (frontaland maximum widths), and considering the vault

morphology in terms of frontal and parietalchords (type I-based landmarks) as well asfunction-independent variables (type III-basedvault heights).

Considering the convergence of the results fromtwo- and three-dimensional approaches, the use ofboth geometric and anatomical landmarks arenecessary to a full complementary discussion onendocranial shape evolution.

Human brain evolution in the Middle Pleistocene

Figure 6 synthesises the major differencesbetween four indicative specimens, namely theSale configuration (African Middle Pleistocene)warped into Zhoukoudian III (Asian MiddlePleistocene), La Chapelle-aux-Saints (EuropeanWurmian Neandertal) and Vatte di Zambana(European Mesolithic modern human). Theyrepresent just indicative morphotypes, and thecomparisons are not necessarily intended to bephylogenetic representations. Sale is considered asreference because of the general plesiomorphendocranial (Holloway, 1981b) and ectocranial(Hublin, 2002) morphology, associated with itsgeographical localisation. The patterns of varia-tion described in this analysis will be discussedaccording to each main endocranial districts.

Frontal area. The frontal lobes have beensuggested to have a major role in humanevolution, because of an interesting developmentin those morphotypes hypothesised to be theearliest representatives of the genus Homo, andformerly included in the hypodigm of Homohabilis (Holloway, 1995; Tobias, 1995). In thefrontal lobes the coronal diameters increase inthe more derived taxa, mostly by means of thedevelopment of the 3rd frontal circumvolutions(Grimaud-Herve, 1997). Actually, what seemsmore interesting is the development of the frontalwidth compared to the maximum (parieto-tempo-ral) breadth. This ratio increases in larger endo-casts, following an allometric pattern sharedwithin the whole genus. In larger hominids it leadsto an allometric expression and development ofthe Broca’s cap, while in the opposite directionleads to the typical frontal narrowing of thearchaic phenotypes.


Fig. 6. Distortion grids showing differences in 2D left lateral configuration between the hypothesised less derived phenotype (Sale)

towards three representative specimens (Zhoukoudian III, La Chapelle aux Saints, Vatte di Zambana), with a draw of the respective

endocasts. Note that this comparison is aimed at a description of the main morphotypes, and does not represent any phylogenetic

hypotheses.

Concerning the frontal vertical development,the anterior midsagittal brain profile has beenhypothesised to have undergone a long stasis sincethe Middle Pleistocene, independently from thelarge variations of the outer bony morphologyrelated to the brow ridge and associated structures(Bookstein et al., 1999). The analyses of theinterlandmark and landmark data here showa general size-related vault elevation, particularlyat the level of the ascending frontal circumvolu-tion, with the archaic Asian specimens showingmore pronounced flattening. This pattern iscombined with a backward shifting of the Rolan-dic scissure, with consequent relative lengtheningof the frontal lobe. Comparable results were

obtained by superimposition of averaged three-dimensional configuration of the endocasts (Bru-ner et al., 2003). Therefore, even if only someminor variations are recorded in the frontalprofile, its shape is nevertheless influenced by sizeand by a generalised vertical stretching, andabsolute stasis is improbable considering theencephalisation processes. Conversely it may bestated that, if the frontal shape differences inextinct human taxa are considered only as theconsequence of brain enlargement, it should bepossible to hypothesise an ‘‘allometric stasis’’, asshape variations along a plesiomorph size-dependent morphological trajectory. The term‘‘allometric stasis’’ is used here to indicate


evolutionary changes mainly based on a non-derived structural system, thus shape variationswithout major neomorphic relationships. Themorphology changes, while the biological modeldoes not (at least concerning a large percentage ofvariability). In any case, in modern humans thegeneralised endocranial convolution involves a rel-ative shortening of the frontal pole that reducesthe effect of the allometric stretching. This result,although secondarily induced by the parietaldevelopment, must also be taken into account.

It should be emphasised that in this study theAsian variability was included, and the frontalarea was entirely considered (until the Rolandicscissure). In Bookstein et al. (1999) the Asian taxawere not considered and only the shape of theanterior cranial fossa was taken into account.Therefore, in the present analysis the Asianspecimens may have increased the size-relateddifferences, which moreover may be situated moreat the frontal ascending circumvolutions than inthe prefrontal cortex housed in the anterior cranialfossa. This volume is further reduced by the post-orbital (backward) shifting of the frontal lobes insome robust Middle Pleistocene specimens (Seidleret al., 1997). Moreover, in previous work the inner(endocranial) profile was analysed together withthe outer (ectocranial) profile (Bookstein et al.,1999). Extreme variation in the latter profile mayhave obscured the more limited variation in theendocranial shape.

It is worth noting that recent volumetricanalyses show a comparable development of thefrontal lobes in modern humans and apes,considering their specific brain size (Semendeferiet al., 1997; Semendeferi and Damasio, 2000),suggesting an allometric stasis within the Homi-noidea and supporting the hypothesis of a general-ised evolutionary inertia of the frontal lobes. Thismay diminish the importance of these areas duringhuman evolution compared to what has beenhistorically assumed. However, it cannot beexcluded that the trespassing of some size bound-aries could have involved some discrete (emergent)changes in neuro-functional organisation. Consid-ering the role of the frontal circumvolutions inhigher cognitive functions and language, thishypothesis needs to be thoroughly investigated.

Parietal area. There is some evidence suggestingthat changes in the parietal lobes can be involvedin the evolution of early hominids, considering theinformation available on the Australopithecinaeendocasts (Holloway, 1983, 1995; Tobias, 1995).The lower parietal areas are extremely variable inextant Hominoidea, while the upper parietalstructures show wide variation in extinct hominids(Holloway, 1981a). It seems than the parietal areasmaintained a key role in the subsequent radiationof the genus Homo, particularly when modernhumans are considered and compared to theextinct taxa. In general, the whole parietal andtemporo-parietal complex widens in differentlineages as brain size enlarges, along with anassociated decrease of the occipital area (Grimaud-Herve, 1997). All the taxa considered here showa common pattern of size-related parieto-temporalwidening. In contrast, as the brain enlarges theparietal outline shows a negative allometricpattern, leading to a relative shortening of themidsagittal profile and flattening of the upper-posterior areas. The posterior height shows a size-related vertical development of the vault alonga shared trajectory in the non-modern sample. Thehigh level of encephalisation of the Neandertalsexaggerates these patterns, with parietal areas highand wide, but short and flattened. It must be notedthat posterior height (H3) and parietal flatteningare not fully comparable variables, and theyshould not be confused. The parietal developmentconcerns shape, i.e. a more rounded or flattenedoutline, while its height concerns size, i.e. theabsolute elevation above the fronto-occipitalchord. Multivariate traditional metrics has beenused to characterise two different morphologicaltrajectories based on this inverse relationshipbetween brain size and parietal structure, separat-ing modern from non-modern specimens (Bruneret al., 2003). As a result of relative parietalshortening, the brain undergoes a generaliseddorsal bending as it enlarges, and the endocast isflexed upward.

It is useful to evaluate the relationship betweenthe inner and outer cranial surfaces, particularlyconsidering the ectocranial lambdoid flattening ofNeandertals. The Neandertals ontogenetic trajec-tory, compared with the pattern expressed in


modern humans, shows a relative development ofthe lower-lateral neurocranial outer bones anda relative reduction of the upper vault surfaces,particularly at the parietal roof (Ponce de Leon andZollikofer, 2001). This pattern perfectly matchesthe vertical development of the Neandertal brainsassociated with a shortening of the parietal outline:the first process is related to lateral verticaldevelopment, the second to the negative allometricpattern of the upper parietal areas.

The allometric development and the midsagittalparietal shortening lead to a parietal ‘‘dispropor-tion’’: encephalisation involves increased parietalwidths and heights on the one hand, but parietallongitudinal reduction and flattening on the other.It can be hypothesised that this pattern could leadto some structural loss of balance in addition tosome functional constraints. This factors can beincluded in the neural-processing limits related tothe neural architecture (Hofman, 2001). It isinteresting that some analyses of Neandertalfunctional craniology revealed hypostotic traitsand ‘‘ontogenetic stress’’ of the posterior cranialdistricts in these populations (Manzi et al., 1996,2000a; Manzi, 2003), previously described as‘‘morphological instability’’ of the Neandertalparieto-occipital structures (Sergi, 1934, 1944,1948). Taking into account the tight ontogeneticand structural relationship between brain andvault bones (Moss and Young, 1960; Enlow,1990), these results must be carefully consideredwithin the hypotheses on the Neandertals evolu-tionary history.

The modern endocasts show a pattern ofparieto-temporal widening similar to the non-modern specimens. In contrast, the modernmorphotype is characterised by a species-specific(actually autapomorphic) parietal development.The parietal chord lengthens, and the midsagittalprofile grows orthogonal to the outline. Theposterior vault elevation and the parietal longitu-dinal development showed in this analysis areassociated with the upper parietal wideningcharacterising the modern ‘‘housed’’ posteriorprofile. The result of the parietal enlargement,both midsagittally and coronally, is the develop-ment of a more globular brain case. The parietalgrowth involves the approaching of the opposite

areas, namely the temporo-cerebellar and thefrontal ones, with closing of the interposed gaps(sylvian and temporal valleys). Here, this processis termed convolution, and it leads to the species-specific ‘‘globularity’’ of the ectocranial counter-part characterising the modern human populations(Manzi et al., 2000b; Lieberman et al., 2002;Bruner et al., 2004).

It is worth noting that the previous three-dimensional analysis of the endocranial extinctvariability was able to characterise the samepatterns, integrating the changes in the parietalareas with those related to the endocranial widening(Bruner et al., 2003). The present two-dimensionalapproach was necessary to localise and describe theupper bending of the vault, or conversely the actualeffect of the surface convolution, because of thelateral view projection associated with the use ofgeometry-related type II landmarks.

Occipital area. The occipital lobes have beenhypothesised to show a steady reduction duringhuman evolution (Holloway, 1983, 1995), changingfrom a more posterior location (behind the parietalareas) to a more advanced position (under theparietal structures), with the cerebellar poles fol-lowing the same pattern (Grimaud-Herve, 1997).This process involves a rotation of the posteriorcomplex forward and under the cerebral mass. Themetric analysis suggests only a size-related verticaldevelopment, while the geometric morphometricapproach confirms the flattening of the occipitalstructures onto the developing parieto-temporalareas. The relative reduction of the most encephal-ised taxa can explain the greater dominance of theanterior branches of the middle meningeal vessels(Grimaud-Herve, 1997) compared with the posteri-or development of the vascular system in theMiddlePleistocene Asian hominids.

Human evolution and brain size

Brain size is surely the most well-known subjectin studies of human brain evolution. Presently,there is no agreement on the dynamics of changesin cranial capacity during the Middle Pleistocene.After the evolution of the early Homo morpho-types, a stasis may have occurred in the enceph-alisation process, with limited brain size increase


until after 600 ka (Ruff et al., 1997). The followingbrain enlargement in different human lineages ledgradually to brain sizes included in the non-pathological lower values of the modern range(Conroy et al., 2000). In contrast, althougha gradual increase of the cranial capacity isreported for the (mostly Asian) Homo erectuspopulations, there is some evidence of a discretetransition to higher cranial capacity values in the(mostly Afro-European) Homo heidelbergensislineage (Rightmire, 2003).

Independently from the degree of encephalisa-tion as quantitative development of the cranialcapacity, the available data from the presentanalyses strengthen and improve the character-isation of two distinct allometric trajectoriesdescribed for the evolution of the human brain(Bruner et al., 2003). It must stressed here that theterm trajectory is interpreted as a general size-related shape change. Thus it is a structuralrelation between cerebral shape and encephalisa-tion. It is therefore not assumed to be ‘‘geometric’’allometry (i.e. the analysis of the departure fromisometric scaling), and inferences concerning thequantification of these trajectories have not beenconsidered because of the small number of speci-mens in each operational group. Furthermore,trajectory is obviously not used here to implya progressive evolutionary process.

The vertical endocranial development (proba-bly stressed at the level of frontal ascendingcircumvolution), the frontal and temporal widen-ing, and the occipital flattening, represent commonsize-related consequences shared within the genusHomo. Conversely, the non-modern taxa arecharacterised by a parietal shortening and flatten-ing, while the modern specimens show a derivedstructural configuration based on a parietal hy-pertrophy involving a convolution of the endo-cranial morphology.

Therefore, Neandertals are hypothesised to bederived on the basis of the allometric expressionand the encephalisation degree (quantity), butplesiomorphic on the basis of structural andfunctional processes (quality). In any case, majorshared allometric trajectories do not exclude thepossibility of minor species-specific changes. Itmust be noted that in Neandertals a certain degree

of parasagittal parietal development has beendescribed, shifting the tent-like posterior profileof Homo erectus andHomo heidelbergensis into theclassic en bombe outline (Bruner et al., 2003).Other differences have been proposed as endocra-nial autapomorphic features of the Neandertallineage, e.g. the high frequency of a well developedspheno-parietal sinus (Gracia, 1991; Saban, 1995;Arsuaga et al., 1997; Grimaud-Herve, 1997).However, considering the presence of this trait inthe Indonesian and Zhoukoudian Homo erectus(Grimaud-Herve, 1997) and the scaling relation-ship between archaic groups and Neandertals, itmust be verified whether or not the expression ofthis trace could be another result of the allometricstructural vector.

Concerning the variation in Homo sapiens,some differences can occur between Late Pleisto-cene and Holocene populations. Metric analyseshave shown that Upper Paleolithic modern hu-mans display increased heights and lengths anddecreased widths with respect to recent endocrania(Grimaud-Herve, 1997). These differences could beinterpreted in terms of the allometric trajectory ofthe Holocene gracilisation and decrease of cranialcapacity (Henneberg, 1988; Holloway, 1995; Ruffet al., 1997), but further analyses must beaddressed to this issue.

Clearly, this study is limited to the endocranialgeometry, and the results must be interpreted interms of structural macroscopic pattern. Noinformation is available on the architecture ofthe cerebral tissues, that can be just hypothesisedon neontological bases. For instance, it has beensuggested that hominid evolution may have beenrelated to a specific neocortical expansion morethan a general brain size increase, with departurefrom the non-human allometric trajectories infrontal and temporal white-matter development(Rilling and Insel, 1999; Rilling and Seligman,2002).

Brain evolution and functional morphology

The geometry of the brain should be interpretedas the functional and structural result of a bio-mechanical complex. Morphology is the finalresult of forces and intensities which originate


from the interactions between genetic programsand the individual environment. Yet they developwithin a physical medium that is an active part ofthe process by means of its mechanical constraints,leading to the final configuration of the structures(Thompson, 1942; Moss and Young, 1960). Thisapproach is the basis of a dynamic conception ofcranial morphology, in which evolution andontogeny can be interpreted as the products ofstructural balances (Sergi, 1934, 1944; Enlow,1990).

The endocranial cavity, formed by the cerebralcapsule, the skull base and the meninges, isa functional matrix sensitive to the influence ofthe growing soft tissues (Moss and Young, 1960).The neural mass determines the force and magni-tude of growth (quantity), while the skull base, thedural layers and the endocranial tensors (falxcerebri and tentorium cerebelli) represent vectors ofdirection controlling the qualitative result (shape).The vault bones show a passive growth mecha-nism, in which bone deposition and resorption areinduced by the soft tissue stimulated by the brainpressure and bone separation at the sutures(Enlow, 1990). In contrast, the skull base compo-nents and the three endocranial fossae growactively by drift, displacing the surroundingsplanchnocranial and basicranial structures. Thesepatterns of growth suggest possible explanationsfor the allometric trends hypothesised in thispaper.

The frontal lobes seem to be more conservativeduring hominid evolution with respect to othercerebral districts. The vertical development islimited, with the frontal areas growing mostlylaterally. There are at least two constraints to thevertical development. First, the maximum loadingof the frontal lobes onto the orbital roofs may belimited by their structural resistance. Second,a general vertical development of the anteriorfossa leads to a downward rotation of the orbits,of the nasomaxillary complex and of the olfactorybulbs (Enlow, 1990). After a certain degree ofdownward pushing, the process may reach a phys-ical limit beyond which a further displacement ofthe facial volume is not achievable. In contrast,a lateral widening is possible because of theextreme frontalisation of the genus Homo and

the marked splanchnocranial reduction. The firstprocess advances the temporal fossa (Ross, 1995;Ravosa et al., 2000), while the second reduces thevolume of the anterior temporal muscle (Cachel,1978). Interestingly, recent genetic advances onmutations of the myosin in apes and humanssupport a similar evolutionary relationship be-tween the temporal muscle and the neurocranialdevelopment (Stedman et al., 2004).

As a consequence of the orbital frontalisationand muzzle reduction, a large lateral volume isavailable for frontal broadening of the brain,presented in archaic hominids as the post-orbitalconstriction and reduced in later taxa by wideningof the frontal lobes. Thus, the broadening of thefrontal lobes is the only mechanism that is able toenlarge allometrically the frontal areas, given thevertical constraints discussed above. The limitsrelated to the frontal height development and theavailability of lateral enlargement can thus beregarded as compensatory processes. Hemisphericspecialisation is related to size via the positiveallometric increase in connectivity (Hofman,2001). It will be interesting to test whether or notthe rate of the allometric frontal widening couldhave represented a pre-adaptation to the hemi-spheric specialisation at the third frontal circum-volutions.

Even if the frontal lobes were not involved inmajor volumetric or morphological rearrange-ments during human evolution, an increaseddegree of its gyrification has been anyway sug-gested (Rilling and Insel, 1999), and the respectivecognitive consequences are presently not known.

If the anterior endocranial areas may enlargemainly through a lateral widening, the posteriorvolumes are more easily enlarged by a verticaldevelopment. The maximum breadth of the cranialbase has been suggested to have the greatestinfluence on the main cranial proportions (Lieber-man et al., 2000). If a variable is associated witha large number of secondary processes, thenecessity of functional coherence will preservethe character from large deviations.

The parietal areas seem to have a major role inthe structural network of the human endocranialsystem (Fig. 7). It has been suggested that ascranial capacity increases the parietal areas


Fig. 7. Structural hypotheses on two encephalisation trajectories. Endocranial capacity increases independently in modern humans

(top) and Neandertals (bottom). The first process is based upon a neomorphic structural change related to a parietal hypertrophy. The

second is largely based upon the quantitative development of an archaic pattern. The distortion grids show the warp from the mean

archaic shape (here represented by the Sale endocast) to the mean modern and Neandertal configurations (x 1.6).

undergo to a relative shortening and flattening,except when modern humans are compared withnon-modern taxa (this work; Bruner et al., 2003).The longitudinal main tensor of brain develop-ment is the falx cerebri, a meningeal processinterposed between the two cerebral hemispheres.As the brain enlarges, a basic allometric relationdescribes a cubic cerebral volume increasing onthe quadratic meningeal sheet of the falx, oreven along its linear chord projection acting asthe real physical vector on the brain surface.Considering the important structural role ofthe falx cerebri, this process may easily involvea loss of balance and may require some shapeadjustments.

The parietal lobes lie midway between the twobrain extremes, represented by the frontal andoccipital poles. Following the increase in brainsize, the anterior and posterior lobes are free torearrange by means of a different orientation. Incontrast, the parietal area is constrained by itsmiddle position and cannot rearrange the allome-tric pattern by an independent movement. Asa result, while the brain enlarges the falx cerebriand other tensors cannot keep the pace with thegeneral growth, inducing a relative midsagittalreduction. The overall effect could be a parietal

midsagittal shortening and consequent flattening,with a cerebral upward bending related to thetension at the frontal and occipital lobes. It mustbe stressed that also during ontogeny the frontal,temporal and inferior parietal areas undergoa relative increase, while the occipital and superiorparietal districts show a relative stasis (see Pena-Melian, 2000).

The role of the cranial base flexion within thiscontext is of major interest. The cranial base anglehas a determinant role in cerebral spatial packing(Ross and Ravosa, 1993). Although its function inhuman evolution seems to suggest other compen-satory processes, at least in modern humans (Rossand Henneberg, 1995; Jeffery and Spoor, 2002),the role of this variable is not completely resolved(Lieberman et al., 2000; McCarthy, 2001). Thedorsal bending and the parietal convolution pre-viously described is likely to have some effect onthe cranial base angle, and further analyses arerequired to clarify this issue. Both processes shouldaffect the cranial base variation in oppositedirections, the dorsal bending involving a moreplatybasic structure, and the parietal convolutioninducing klinorhynchy. The same convolutionprocess affected and rearranged the vertical de-velopment. A similar scenario to this parietal


scaling hypothesis was proposed by Strait (1999)to be a main factor involved in cranial base flexion,on the basis of the non-cortical brain properties.The ‘‘non-cortical scaling hypothesis’’ suggestsa soft tissue constraint related to the negativeallometric pattern of the medullar, mesencephalicand diencephalic structures, eventually related tometabolic requirements. Regardless of the causalnexus between parietal bone development, bio-mechanical tensors, brain tissues and cranial baseflexion, it is clear that they represent an integratedsystem within a functional network.

During anthropoid brain evolution the neo-cortical white matter has scaled at a higher powerthan the grey matter (Rilling and Insel, 1999;Hofman, 2001). Thus, the number of connections(axons) outpaced the number of neocorticalneurons as the brain enlarged. Functionally, thiscan be interpreted as an increase of informationexchange that is faster than the increase of theinformation itself. It is worth noting that theincreased spherical shape in modern populationsfurther increased the connectivity of the brain’sneuronal network by the shortening of thedistances between the different districts. In a systemthat processes thousands of bits of informationevery few microseconds, a minor increase in flowefficiency can induce an exponential advantage bymean of a decrease of the ‘‘wiring length’’ (see alsoMcCarthy, 2001).

Parietal development in modern humans mustbe integrated within a theory of localised cellsproliferation. According to the radial unit hypoth-esis (see Rakic and Kornack, 2001) such pro-liferation is related to an increase of the sourcecells at the ventricular zone. Recent advances onthe genetic control of cortical folding have beenbased on a group of pathologies generally de-scribed as polymicrogyria (Rakic, 2004). Theseanalyses suggest that even single mutations caninvolve marked and discrete changes in thestructural organisation of specific functional areasof the cortical layers. Consequently, random andlocalised genomic changes can induce a regionalcortical development by addition of radial units,promoting fast and localised evolutionary events.

The development of the parietal areas withrelative adjustment of the overall brain morphol-

ogy and increase of connectivity also fits wellwithin the tension-based theory of brain morpho-genesis (Van Essen, 1997). This hypothesis sug-gests that during neural morphogenesis thephysical tension of the neural structures (axons,dendrites and glial processes) produces mechanicalforces that guide the shape development and‘‘compact wiring’’ of the brain. As in the relation-ship with physical tensors represented by the falxcerebri and tentorium cerebelli, the magnitude ofthe process is again based upon the hydrostaticpressure produced by brain enlargement. Twoalternative inferences may follow. First, themodern parietal development and the conse-quently more spherical brain shape may haveincreased the compact wiring efficiency. If so, theparietal functional development should then beregarded as the major force promoting the changeof brain morphology. On the other hand, somerearrangements based on the functional biome-chanics of the neural tensors may have involveda necessary parietal adjustment. In that case,parietal development was not a direct adaptationbut a consequence of other changes. According toeither explanation, and considering the multifac-torial functions related to parietal development, itis likely that the shift from the non-modernallometric trajectory and the resulting enhance-ment of the parietal lobes had cognitive con-sequences. In other words, results presented heresuggest that the parietal development in modernhumans is the only non-allometric differencebetween Homo sapiens and non-modern taxa,and this morphological change probably may haverepresented a discrete cognitive shift.

The parietal cortex may have had a principalrole during hominid evolution through its directrelationship with visuospatial integration, sensoryintegration, multimodal processing, and socialcommunication (Holloway, 1995; Faillenot et al.,1999). The parietal lobes are involved in thecontrol of finger movements during spatial anal-ysis (Shibata and Ioannides, 2001) and in turn acton cognitive tasks and association processes(Culham and Kanwisher, 2001). It is interestingthat the parietal districts seem to be crucial inmanipulation and planning of motor sequencesbecause this suggests a role in tool-making. In this


perspective, it is likely that the discrete qualitativedevelopment of operational objects displayed inthe Late Pleistocene by modern humans wasrelated to such a structural transformation. Inaddition, hypotheses about the evolution oflanguage have been based on a comparisonbetween speech and tool-making activity, bothrepresented by the modular organisation of motorsequences (see Bradshaw, 1997). In 1973 KonradLorenz interpreted the roots of the conceptualthinking by means of five variables: together withabstraction, curiosity, voluntary movement, andimitation, he listed the spatial orientation (Lorenz,1973). In particular, he referred to the potentialityto create an ‘‘imagined space’’ interior to thecentral nervous system. This space works asa model to act virtually within an environmentby means of the thought, and it is supposed torepresent a basic foundation of any conceptualoperation, including language. Considering thehypothesised role of the parietal areas in visuo-spatial integration as recognition and communi-cation of the external environment, the evolutionof these structures may be directly related to theevolution of such ‘‘inner reality’’.

Finally, by means of the parietal expansion themodern human brain acquired a more globularshape, and the relative decrease of the cerebralsurface area with respect to brain volume isdirectly related to thermoregulation and metabolicbudget, and secondarily to diet and behaviour(Leonard and Robertson, 1992, 1994, 1997; Aielloand Wheeler, 1995; Kaplan et al., 2000; Leonardet al., 2003).

Although the present analysis suggests a majorrole of the parietal areas during human brainevolution, it must be stressed that other cerebraldistricts - e.g. the temporal and the cerebellarstructures - are more difficult to consider in thefossil record but provide interesting perspectivesfor future studies (see Semendeferi, 2001; Weaver,2002). For human brain evolution, the structuraland functional morphology can be interpreted asa single and complex ‘‘phylogenetic package’’(Enlow, 1990). The neuro-functional consequencesof the development of specific cortical areas andthe change in spatial organisation between differ-ent districts, and possibly of metabolism, suggest

that a discrete cognitive shift between non-modernand modern humans cannot be excluded.

Acknowledgements

I am sincerely grateful to Giorgio Manzi, whowas a constant reference during this project. JuanLuis Arsuaga, Patricio Dominguez, and AnaGracia gave me the opportunity to begin thiswork with useful suggestions and help. Henry andMarie-Antoinette de Lumley, and Aldo andEugenia Segre, allowed the study of most of thespecimens. Dominique Grimaud-Herve was theprecious teacher who introduced me to paleoneur-ology. Dennis Slice had the patience to help meevery time I got entangled with multivariatequestions. Bernard Wood and Fabio di Vincenzofurnished interesting cues. Christoph Zollikoferand Charles Lockwood provided many usefulcomments during the review process. Two anon-ymous reviewers supplied important advice andhelped to consider a wide and varied literature.Maryanne Tafuri helped in the final linguisticrevision. This project was carried out at theLaboratory of Human Paleontology directed byP. Passarello at the Universita ‘‘La Sapienza’’,Roma. This work was partly supported by theItalian MIUR/urst (including COFIN grants).

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