Evolution of the Base of the Brain

8/10/2019 Evolution of the Base of the Brain

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1NATURE COMMUNICATIONS | 2:588 | DOI: 10.1038/ncomms1593 | www.nature.com/naturecommunications

2011Macmillan Publishers Limited. All rights reserved.

Received 16 May 2011 |Accepted 14 Nov 2011 |Published 13 Dec 2011 DOI: 10.1038/ncomms1593

The increase of brain size relative to body sizeencephalizationis intimately linked with human

evolution. However, two genetically different evolutionary lineages, Neanderthals and modern

humans, have produced similarly large-brained human species. Thus, understanding human

brain evolution should include research into specific cerebral reorganization, possibly reflected

by brain shape changes. Here we exploit developmental integration between the brain and its

underlying skeletal base to test hypotheses about brain evolution in Homo. Three-dimensional

geometric morphometric analyses of endobasicranial shape reveal previously undocumented

details of evolutionary changes in Homo sapiens. Larger olfactory bulbs, relatively wider

orbitofrontal cortex, relatively increased and forward projecting temporal lobe poles appear

unique to modern humans.Such brain reorganization, beside physical consequences for overall

skull shape, might have contributed to the evolution of H. sapiens learning and social capacities,

in which higher olfactory functions and its cognitive, neurological behavioral implications could

have been hitherto underestimated factors.

1Paleoanthropology Group, Department of Paleobiology, Museo Nacional de Ciencias Naturales, CSIC. J. G. Abascal 2, 28006 Madrid, Spain. 2Department

of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany. 3Departamento de Anatoma

y Embriologa Humana I. Facultad de Medicina, Universidad Complutense de Madrid, Madrid, Spain. 4Dipartimento di Biologia Ambientale. Sapienza

Universit di Roma, Piazzale Aldo Moro 5, 00185 Rome, Italy. 5Paleoanthropology, Department of Early Prehistory and Quaternary Ecology and

Senckenberg Center for Human Evolution and Paleoecology, Eberhard Karls Universitt Tbingen, Rmelinstr. 23. 72070 Tbingen, Germany. 6Department

of Paleontology, Natural History Museum, Cromwell Road, London SW7 5BD, UK. Correspondence and requests for materials should be addressed to

M.B. (email: [email protected]).

Evolution of the base of the brain in highly

encephalized human species

Markus Bastir1, Antonio Rosas1, Philipp Gunz2, Angel Pea-Melian3, Giorgio Manzi4, Katerina Harvati5,

Robert Kruszynski6, Chris Stringer6& Jean-Jacques Hublin2


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NATURE COMMUNICATIONS | DOI: 10.1038/ncomms1593

NATURE COMMUNICATIONS | 2:588 | DOI: 10.1038/ncomms1593 | www.nature.com/naturecommunications


Accumulated palaeontological knowledge has established thatthe genus Homohas diversied in the last 2 million years intoseveral evolutionary lineages, among which at least Nean-

derthals (H. neanderthalensis) and modern humans (H. sapiens)have independently and in parallel evolved a large brain, on averageabove 1400 cm3(res 16). Clariying the diversity in H. sapiensbrainorm is thereore essential or understanding cerebral evolutionand unctions3,4,7,8.

Te orm o the base o the brain is well reected in the shape o

the endocranial skeletal base9supporting rontal lobes and olactorybulbs within the anterior cranial ossae (ACF), and temporal lobeswithin the middle cranial ossae (MCF). During prenatal ontogenythe inner and outer layers o the ectomeninx, covering the develop-ing brain, differentiate into dura materand into precursors o thechondrocranium, which later ossies into the endocranial base9,10.Moreover, the shape o the cribriorm plate directly reects themorphology o the olactory bulbs, as they develop jointly9,11.

aking advantage o these intimate embryological and anatomicalrelationships, we assessed shape differences in the cranial base amonglarge-brained humans (able 1). Specically, we inspected the ACFto assess whether rontal widening in highly encephalized modernH. sapiensand Neanderthals differed in shape and pattern6,12. MCFwere analysed to test whether modern humans evolved specically

enlarged temporal lobes2,1316. Tese hypotheses were addressedby geometric morphometrics17o three-dimensional (3-D) suracelandmarks o the associated endocranial cerebral base conguration(Supplementary Fig. S1; Supplementary able S1).

ResultsPrincipal patterns of size and shape variation. Principalcomponents (PCs) analysis o size and shape17 shows large-scalepatterns o variation and overall distributions o data (Fig. 1). PC1distinguishes the non-human sample rom Homo(Fig. 2a,b). PC2polarizes early Homoversus modern humans (Fig. 2c,d). Large-scaleshape differences show that in chimpanzees, the endocranial baseo the brain is narrow, oval and elongated with a long presphenoidand a very short cribriorm plate (Fig. 2a). In Homo (Fig. 2b) the

base o the brain is wider and rounded, with an elongated cribriormplate and a relatively shortened pre-sphenoid. Early Homo(Fig. 2c)is characterized by a triangular endocranial base o the brain with ashorter cribriorm plate; modern humans (Fig. 2d) by a rectangularbase o the brain with an elongated cribriorm plate. Figure 3illustrates the mean shapes within Homospecies.

Te covariance within the chimpanzee and hominin clouds in thePC1PC2 plots (Fig. 1) reects the importance o size increase and

allometry in brain and evolution o the base o the brain. Distribu-tions o archaic and modern humans are roughly parallel reectingdifferent scaling patterns shown previously6. Evolutionary trajecto-ries are indicated by lines originating close to early Homoheadingtowards the centres o the distribution. Te Neanderthal trajectorypasses in the vicinity o Petralona, a European Middle Pleistocenespecimen, whereas the modern human trajectory passes throughthe vicinity o Arican Middle Pleistocene humans (Bodo, BrokenHill).

For analysis o non-allometric evolutionary actors, multivari-ate regression analyses were perormed, indicating that allometryaccounts or ~42% o variation (P= 0.001) in the total sample and~2.5% within Homo(P= 0.007). Non-allometric eatures o brain andendocranial evolution in Homowere urther analysed by mean shapecomparisons o the non-allometric regression residuals (able 2).

Statistical assessment of hypotheses. Permutation tests o groupmembership (N= 10.000) were used to statistically assess differ-ences in Procrustes distance1820 between non-allometric meanshapes o H. sapiensand other Homospecies. Neanderthals differedsignicantly rom the early Homo average and modern humanswere highly signicantly different rom all other Homo species(able 2). Procrustes distance (able 2) quanties the overall differ-

ence between means o registered landmark congurations17. Teaverage distance between means within modern human popula-tions (d= 0.037) was ~25% smaller than between modern humansand Neanderthals (d= 0.049). However, biological understand-

0.10

0.05

0.00

0.05

0.100.40 0.30 0.20 0.10 0.00 0.10 0.20 0.30

KNM ER 3883

KNM ER 3733

Ka

Bo Sa

PeCh

GuCi

Si

Fe

SkFq

Ml

P.trog

H.sap

H.nean

MPLHomo

EarlyHomo

H.sap.fossil

Figure 1 | Principal components (PC) analysis.Distributions of species

along principal component (PC)1 (78.9% of total variance) and PC2 (3.4%

of total variance). PC1 (abscissa) polarizes chimpanzees (negative scores)

from Homo(positive scores); PC2 (ordinate) polarizes early Homo(positive

scores) and modern humans (negative scores). Abbreviations for fossils

Ka: Broken Hill; Bo: Bodo; Pe: Petralona; Sa: Saccopastore 1; Ch: La Chapelle

aux Saints; Gu: Guattari 1; Fe: La Ferrassie; Fq: Forbes Quarry; Si: Singa; Sk:

Skhul V; Ml: Mladec 1 Ci: Cioclovina. Note divergent evolutionary patterns

(indicated by arrows: dashed arrow indicating Neanderthal evolutionary

lineage; dotted arrow showing modern human evolutionary lineage).

Arrowheads are placed towards the centres of the Neanderthal and

modern human distributions.

a b c d

Figure 2 | Principal patterns of form variation.(a) Shape associated to

negative PC1 scores; (b) shape associated to positive PC1 scores; (c) shape

associated to positive PC2 scores; (d) shape associated to negative

PC2 scores.

Table 1 | Fossil specimens. All computed tomography data

except where stated STL: stereolithography).

Fossils Group

KNM-ER 3883 H. ergaster (earlyAfrican

H. erectus),early Homo

KNM-ER 3733 H. ergaster (earlyAfrican

H. erectus),early Homo

Bodo Midpleistocene Homo

Broken Hill (Kabwe) Midpleistocene Homo

Petralona (STL) Midpleistocene Homo

La Ferrassie 1 H. neanderthalensis

La Chapelle-aux Saints 1 H. neanderthalensis

Saccopastore 1 H. neanderthalensis

Guattari 1 H. neanderthalensis

Forbes Quarry H. neanderthalensis

Singa H. sapiensfossil

Skhul V H. sapiensfossil

Mladec 1 H. sapiensfossil

Cioclovina59 H. sapiensfossil


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ing o these quantitative results required detailed analysis o thecorresponding visualizations o the involved anatomical structurespresented in Figure 4.

Frontal lobes and olfactory bulbs differ in large-brained humans.o investigate the evolution o the ACF, and the morphology othe associated basal part o the rontal lobes12we calculated thin-plates spline transormation grids (PS-grids)17between the non-allometric species averages. A yellow PS-grid passes through the

limit between anterior and MCF and the anterior- and superior-most landmarks o the orbital roos (Methods). Modern humansevolved a unique endocranial conguration at the basal rontallobes. When compared with early Homo(Fig. 4a), the ACF-grid isstrongly expanded mediolaterally (Fig. 4b). Frontal lobe widening,known or higher encephalized humans6,12, produces a rectangularoutline o the rontal lobe base in H. sapiens. Maximum breadtho the basal rontal lobes is located close to the anterior hal o theACF (Figs 3,4b) at the level o the cribriorm plate. At the same timethe cribriorm plate in the centre o the ACF, is relocated by poste-rior expansion. It is thus relatively larger than in early Homoandshifs the central midline base relatively backwards. Te backward-exed vertical PS-grid (Fig. 4b) and the expanded white PS-grid(Fig. 4k) shows this clearly (Supplementary Movie 1).

Neanderthals are also expanded mediolaterally but differentlywhen compared with H. sapiens.Te greatest width o the base othe rontal lobes was at the posterior hal o the ACF, posterior tothe cribriorm plate. Further, the cribriorm plate (and olactorybulbs) was slightly increased anteriorly leading to a more oval ACFoutline (Fig. 4c,l; Supplementary Movie 2). (Tese different evolu-tionary patterns were also ound comparing Mid-Pleistocene ossilswith modern humans and Neanderthals, Supplementary Fig. S2.)

Te signicantly different evolutionary patterns in the modernhuman and Neanderthal lineages are shown in Figure 5. In H. sapienscribriorm expansion has occurred posteriorly. Tis leads to anendocranial retraction o midline base structures relative to thelateral ACF, which projects orwards more and is relatively wideranteriorly (Supplementary Movies 3 and 4). In Neanderthals,

cribriorm expansion is weaker and occurs anteriorly. Te lateralACF is retracted relative to the midline, which is rather stable.

Cribriorm plate enlargement in H. sapienswas urther assessedcomparing the lengths o the cribriorm plate o three Neander-thals (Forbes Quarry: 17 mm; Saccopastore 1: 17.5 mm; Guattari 1:23.3 mm; average: 19.16 mm) with H. sapiens(average: 22.32 mm).Owing to the small sample size o Neanderthals, non-parametricstatistics were used to test the null hypothesis that cribriorm lengthmeasurements rom Neanderthal and modern humans were drawn

rom the same population. Signicant differences at a P= 0.0019level (z-adjusted P= 0.025) suggested larger cribriorm plates andolactory bulbs in modern humans.

Shape differences in the basal rontal lobes can either relate to thelarger cribriorm plate due to integration, or may imply increasedneuroglia, known in primate encephalization18,19, increased gyri-cation20or increased numbers o mini columns21. Number andwidth o these, and the space between them available or intercon-nectivity have been discussed in the context o higher cognitiveunctions related to prerontal cortex21, among other eatures2225.More importantly, arrangement o mini columns distinguishesH. sapiens rom great apes21, in contrast to relative rontal lobevolume, which does not differ among hominoids14,15,21.

However, evolutionary shape changes at the base o the rontal

lobes shown in Figure 4 support the hypothesis o a rontal widen-ing in higher encephalized members o Homo12. Nevertheless, oursurace analysis reveals local differences o widening, adding spatialdetail to recent allometric rontal lobe comparisons12.

Modern human temporal lobes have an apomorphic location andsize. emporal lobe morphology was approximated by quantica-tion o 3-D endocranial surace shape o the MCF9,10,16. o visualizethe results o quantitative non-allometric mean shape comparisonsa red PS-grid was positioned through the orward-most projectiono the MCF poles, which correspond to the poles o the temporallobes16. Te posterior position o the PS-grid was dened by land-marks at the base o the petrosal pyramids26.

ransormations o the MCFPS-grid (Fig. 4a,d,j into

Fig. 4b,e,k) visualize main patterns o MCF-temporal lobe evolutionin modern humans. Tese evolutionary changes include a strongincrease in relative length, seen as anteroposterior expansion othe MCF grid (Fig. 4b). Modern human temporal lobes are anteri-orly also relatively wider (although both large-brained humans showincrease in MCF width). Increased relative width o the anterior-most poles o the temporal lobes has been hypothesized2,27. Ourdata quantiy the entire conguration o the temporal lobe polesand show that temporal lobe increase in width in modern humanshas not only occurred medially to the anterior-most poles but alsosuperolaterally (Fig. 4b; Supplementary Movie 1). Elevation o thered MCF grid in modern humans (Fig. 4e) suggests relative increasein height. As a result, relatively longer, wider and higher modernhuman temporal poles project orwards relative to the midline16,

shown by the anterolateral expansion o the vertical PS-grid(Fig. 4b), but more clearly by bilateral orwards deormations o thevertical PS-grid in ront o the temporal lobe poles (Fig. 4k). Te

Early Homo

a b c d

Midpleistocene Homo H. neander thalensis H. sapiens

Figure 3 | Endocranial mean shapes.(a) Early Homo; (b) Midpleistocene

Homo;(c) H. neanderthalensis; (d) H. sapiens. A modern human

endocranium was used to visualize the means shape by warping its

endocranial surface model onto the landmark configurations of several

species means. Note differences in the outlines relating to frontal and

temporal lobe shapes. (a) Triangular, (b) Circular, (c) Oval,

(d) Rectangular.

Table 2 | Non-allometric mean shape differences in Procrustes distance (d) and significance levels (see also Supplementary Table S2).

Early Homo Midpleistocene Homo H. neanderthalensis

d P-value d P-value d P-value

Midpleistocene Homo 0.098 0.105

H.neanderthalensis 0.091 0.047 0.071 0.0002

H. sapiens 0.106 0.000 0.078 < 0.0001 0.050 < 0.0002

Bold numbers indicate P< 0.05.


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retracted area o the vertical grid in the midline is due to posteriorcribriorm expansion (Fig. 4k; Supplementary Movie 1).

In contrast to modern humans, Neanderthal temporal lobe shapeevolution does not comprise a relative elongation and orwardsdeormations o the vertical PS-grid (Fig. 4c,l). Tere is increasein relative width but MCF poles remain vertically low, similar to theprimitive condition (Fig. 4d,; or example, early Homo; Supplemen-tary Movie 2). Retention o low temporal pole position and rela-tive length could be seen as structural elements o Bruner et al.s6hypothesis o an archaic pattern o Neanderthal encephalization.

Net effects o these distinct evolutionary patterns are shown inFigure 5 (Supplementary Movie 3 and 4). PS-grid transormationso H. sapiensinto Neanderthals (Fig. 5a,c,e,g) and Neanderthals intoH. sapiens(Fig. 5b,d,,h) show that modern humans still have signi-icantly orward-projecting temporal lobe poles, that are also shifedmore laterally and are still vertically increased (Fig. 5c,d). Ineriorviews demonstrate well decreased lateral width and projection

in Neanderthals (Fig. 5g) compared with H. sapiens(Fig. 5h). Strongretraction o the midline base (sphenoid) due to posterior cribri-orm enlargement in the transormation o the Neanderthal into themodern human mean (Fig. 5h) leadswhen transorming modernhumans into Neanderthalsto a comparably strong orwards shifo the central cranial base in the latter (Fig. 5g).

Our results conrm quantitatively previous speculationsbased on partial measurements on temporal lobe evolution inHomo2,13,16,2728. Importantly, the mid-sagittal part o the modernhuman endocranium is in a more posterior position (Fig. 5g,h).

H. neanderthalensis H. sapiens

a b

c d

e f

g h

Figure 5 | Non-allometric differences between modern humans and

Neanderthals.Shown as H. sapiens- Neanderthal (left column) and

Neanderthal - H. sapiens(right column) transformations (both 1.5

magnified). From uppermost to lowest row: superior, lateral, frontal and

inferior views are shown. (a), (c), (e), and (g) Neanderthals; (b), (d), (f)

and (h) H. sapiens. Note that differences are mainly recognizable in the top

(a,b), lateral (c,d) and inferior (g,h) views showing lateral expansion at the

ACF at the anterolateral prefrontal cortex, significantly stronger vertical

and lateral increase and forwards projection of the MCF-temporal lobe

poles and enlarged cribriform plate and olfactory bulb (TPS-grid in white)

in modern humans, causing a backwards retraction of the pre-sphenoid

and sella turcica(gcompared with h).

a b c

d e f

g h i

j k

Early Homo H. sapiens H. neanderthalensis

l

Figure 4 | Evolutionary transformations of mean shapes after allometry

adjustment.Left column: early Homo; middle column: H. sapiens; right

column: H. neanderthalensis. Yellow TPS grid visualizes shape change of

ACF and basal frontal lobe complex; Red TPS-grid shows changes at MCF

and temporal lobe complex; Dark-blue TPS-grid (vertical) delimits anterior

and MCF and their associated cerebral parts. White TPS grids illustrate

non-allometric evolution at the cribriform plate and olfactory bulbs. (a)

Top view of undeformed early Homomean; (b) transformation of (a) into

H. sapiens; (c) transformation of (a) into H. neanderthalensis. (d) Lateralview of undeformed early Homomean. (e) Transformation of (d) into

H. sapiens, (f) transformation of (d) into H. neanderthalensis; (g) frontal

view of undeformed early Homo; (h) transformation of (g) into

H. sapiens; (i) transformation of (g) into H. neanderthalensis. (j) Inferior

view of undeformed early Homomean. (k) Transformation of (j) into

H. sapiens. (l) Transformation of (j) into H. neanderthalensis; note

different TPS transformations pattern in early Homo-H. sapiensand early

Homo -H.neanderthalensiscomparisons. (Shape difference vectors

are 1.5 magnified).


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As mentioned previously, differential expansion o the cribriorm plateand olactory bulbs appears implicated in this evolutionary change.

Figure 4 suggests that non-allometric increase o the cribriormlength and o the widths o the rontal lobes and temporal lobe polesare apomorphies in the large-brained human clade (H. sapiens,H. neanderthalensis). In a rontal view, large-brained humans alsoshare a lower midline base relative to the lateral one (Fig. 4g, h, and i).H. sapiens is autapomorphic by a posteriorly enlarged cribriormplate, which shifs the central base posteriorly and roughly inter-

sects with the maximal ACF diameter, and a orward-projection orelatively anterior and superolaterally increased temporal lobe polerelative to the central base (optic oramina; Fig. 4b,e,k). Neanderthalautapomorphies include a cribriorm plate, which is also enlarged,but anteriorly and less so than in H. sapiens, and shifed slightlyanteriorly. Maximum ACF diameter passes posteriorly to the cribri-orm plate (Fig. 4c,j,l).

DiscussionEmpirical evidence has repeatedly demonstrated that a major parto primate brain evolution is explained by brain size increase19,25,29.Our PCs (Fig. 1) and multivariate regression analyses o shapevariation at the endocranial base o the brain likely reect thisallometric actor. Nevertheless, non-allometric eatures have also

been identied (able 2, Fig. 4) that are suggestive o more specicinterpretations19,25.

Evolution in Homois organized around modications o the baseo the brain morphology and supposedly associated unctions. At aunctional level o interpretation, it is clear that not all behaviour-ally relevant evolutionary modications in brain connectivity andstructure will be recorded in shape changes o the brain and endoc-ranium. Our study reveals signicant evolutionary modications othe absolute and relative size o the cribriorm plate, accompaniedby changing congurations o the endocranial base o the temporallobe poles and basal rontal lobes.

However, evolutionary shape change o the endocranium couldalso reect effects o cranioacial integration and, thus, non-cer-ebral actors2,27,30. Tereore, palaeoneurological interpretations

o endocranial morphology must consider this wider spectrum oevolutionary and developmental interactions.Cribriorm plate increase is well observed comparing mean

shapes o modern humans with its putative ancestors (both earlyHomoin Figure 4, and Mid-Pleistocene humans in SupplementaryFig. S2) but also with Neanderthals (Fig. 5). Te size o the cribri-orm plate is driven by the size o the olactory bulbs due to coor-dinated embryological development9,11. Adult morphology o thecribriorm plate is achieved early in ontogeny (4 years in humans9and probably even earlier in Neanderthals due to aster maturationrates31). However, due to this very early maturation ontogeneticchanges o adjacent and surrounding acial structures, growing muchlonger than the cribriorm plate32, are very unlikely to inuence cri-briorm morphology by cranioacial integration. Moreover, the act

that large-aced Neanderthals showed smaller cribriorm plates sup-ports an interpretation in terms o neurological actors rather thanby cranioacial integration. Furthermore, its specic increase in H.sapiens implies a unique evolutionary condition o a large cribri-orm plate atop a nasal cavity within an extremely reduced ace2,27.Afer all, nasal cavity and acial sizes are more related to respirationand mastication than to olaction32.

Cribriorm expansion also explains Lieberman et al.s2sugges-tion that modern humans have increased relative length o the ante-rior cranial base at the midline oor, because that length is com-posed o both, the cribriorm plate and the pre-sphenoid, the lattero which is not distinctive between archaic and modern humans13(Supplementary Discussion).

Other basicranial structures mature morphologically later inontogeny and their interactions with other cranioacial elements are

more complex. For example, the midline basicranium attains adultmorphology around 6 years o age in modern humans3233. Te pri-mate midline cranial base is not only determined by the morphol-ogy o the brain34but also by intrinsic actors o its endocranial pre-cursors9and by acial size35. Although in primates large brains areassociated with more exed cranial bases, larger aces are associatedwith less basicranial exion35, which explains why large-brainedand large-aced Neanderthals have less exed cranial bases thanequally large-brained, but small-aced modern humans35.

Te lateral cranial base (ACF, MCF) matures later in ontogenythan midline structures, although still about 4 years earlier than theace32. Tis dissociation offers potential or morphological interac-tion o the endocranial base with the brain and the neurocraniumon its top, and the ace below30,32. However, the volume o the MCFscales isometrically with that o the temporal lobes27, indicatingdevelopmental integration, which corresponds with their commonembryological origin (ecto- and endomeninx)9,10, and strongly sup-ports neurological interpretations o MCF morphology.

Te association between the rontal lobes and the ACF is lesswell studied. Bookstein et al.36suggested that the shape o the ron-tal lobes in the midline has remained unchanged since the MiddlePleistocene, despite signicant evolutionary modications o acialmorphology. Furthermore Stedman et al.s37data show that genetic

actors o masticatory apparatus and acial development were notlikely relevant or rontal lobe evolution afer early Homo.

More research is needed on the integration between the ron-tal lobes, the ACF, the cribriorm plate and acial morphology(Supplementary Discussion).

At a unctional level, variation o olactory bulbs size is cruciallyrelated to olactory capacity and perormance, which has beenobserved across3841and within42species. Olactory bulb size di-erences are also the morphounctional basis o traditional distinc-tions between macrosmatic and microsmatic mammals regardingsubsistence strategies and other eatures o animal behaviour3841.

In addition, within humans, the capacity o odour thresholddetection and odour identication is correlated positively witholactory bulb size, which is driven by variation in the number o

nerve cells41,42

. Te number o cells relates more to olactory unc-tion than overall volume o the olactory bulbs, which is why Smith(re. 41), personal communication) suggested that in closely relatedorganisms with roughly comparable size and similar overall cribri-orm plate morphology, or in intraspecic comparisons, correc-tion or scaling needlessly complicates unctional interpretations.Tereore, the ca. 12% larger cribriorm plates and associated largerolactory bulbs in modern humans may be suggestive o improvedolactory unction11,42,43, although caution is warranted because othe small Neanderthal sample.

Further comparative anatomical study has reported that increaseo olactory bulb volume relative to brain size correlates withvolume increase in a number o other unctionally related limbicstructures30, located at basal parts o the brain including the temporal

lobes (or example, hippocampus, amygdala).Recent brain mapping research using unctional magnetic reso-nance imaging has shown links between neocortical counterparts oACF and olactory and gustatory unction23. Olactory and gustatoryunction, due to its rewarding characteristics and links to memory,was also suggested to participate in an effective and exible humanlearning system23,43. Moreover, positron emission tomography datao regional cerebral blood ow conrmed involvement o the orbit-orontal cortex in processing emotionally valenced olactory stimuliand decision making22,44. However, the volume o the human ron-tal lobes does not apparently differ rom that o other hominoids,taking allometric scaling into account1415, although some evidencestarts to emerge that shape (and not volume) is relevant to brainunction at specic structures45. Whether shape differences at thebasal rontal lobes o large-brained humans (Figs 4 and 5) reect


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different unctional eatures or are consequences o cranioacialintegration must remain speculative and requires urther investi-gation (Supplementary Discussion). Currently, developmental andevolutionary interactions between the rontal lobe base at the ACFand the cribriorm plate may be the saest assumption.

However, the coincident evolutionary changes o structurescomprising olactory neuro-circuitry could be a novel eature inthe evolution o H. sapiens, and, i conrmed, may have inuencedsome eatures o human behaviour. Te olactory neurological cir-

cuitry is highly integrated in cerebral, behavioural and immuno-logical unctions44,46. Following the initial sensory process, axonsrom thousands o cells expressing odour receptors in the mucosao the nasal cavity converge via the cribriorm plate in the olac-tory bulb3841. From there, olactory signals are transmitted to theolactory cortex (rhinal, pyriorm cortex, medioventral to temporallobe poles) and become relayed, on the one hand to higher corticalregions, where conscious thought processes are handled, and on theother hand to the limbic system, where emotional context is gener-ated38,4344. Olactory inormation thus projects to regions criticalor mating, emotions, and ear (amygdala) as well as or motivation,high-level cognitive and emotional processes (orbital prerontal cor-tex). It, thus, serves a role in central nervous system unction aboveand beyond smell46,47. In that respect, olaction differs rom other

sensory modalities. Odour immediately triggers strong emotionalevocations and provokes higher memory retention (Marcel ProustPhenomenon) due to anatomical overlap o structures involved inmemory process and olaction pathways43. Such associations withcognitive processes have been termed by Savic44 higher olactoryunctions. Smell, and linked higher olactory unctions, can thusbe involved in modulating many different aspects o human behav-ior43,44,46,47. It has been reported that people who are congenitallydea or blind have intact reproductivesocial capacities, whereasindividuals with congenital anosmia usually do not43.

Moreover, olaction has been linked to the immunological sys-tem46. It is speculated that odour might be an important actor oattractiveness, that is, a mate selection criterion in human emales,possibly selected or improving immunological tness o the

offspring, or example, in the case o the major histocompatibilitycomplex46,48. Other recent research suggests that humans are alsoable to detect the scent o ear49, potentially important in humansocial interaction.

Bruner et al.6suggested that Neanderthals possessin generalan encephalized (enlarged) version o a primitiveHomobrain by beingat the endpoint o an archaic allometric trajectory, signicantly differ-ent rom the modern human brain scaling trajectory6. On the otherhand, a more localized study revealed also the width o the Neander-thal rontal lobes to be non-allometrically increased12. Our resultsmay t with these observations. Figure 1, indicating roughly paralleldistributions o archaic and modern human scatters, likely reectssome o these general differences, and resembles plots o Bruneret al.6Different scaling also seems consistent with recent studies o

endocranial development showing that Neanderthal brains grew di-erently early in ontogeny, and probably prenatally, when comparedwith modern humans7. Evolutionary differences comprise the entirecranioacial system7,50,51. Detailed basicranial comparisons betweenNeanderthals and modern humans have been missing so ar and ourstudy lls that gap. On the basis o previously mentioned investiga-tions, and also the ndings o this study, it is hypothesized that theirsmaller olactory bulbs (Fig. 5g,h) relate to differences in scalingpatterns between Neanderthals and modern humans6,7.

Our ndings support previous hypotheses6,7 that modernhumans show a different evolutionary trajectory because o theremaining signicant shape differences between Neanderthals andH. sapiensafer allometric size adjustment (Fig. 5, able 2).

Different evolutionary patterns likewise emerge rom compara-tive genetic analyses, whichamong other aspectshave shown

evidence or positive selection o genes related to cognitive develop-ment, that occurred afer the split o H. sapiensand Neanderthals5.Te same applies to roughly 4% o the 78 amino-acid congura-tions, whichancestral in Neanderthalsare directly related tothe olactory system5. Differences in the conguration o the olac-tory sensory apparatus, and its previously discussed involvementinto higher olactory unctions in social, and cognitive (memory)aspects43,44,47could be part o this evolutionary process.

Care should be taken when interpreting our ndings by invoking

evolutionary mechanisms that might have avored a better capacityo smell in modern humans compared with Neanderthals in a wayanalogous to macrosmatic and microsmatic mammals3941. Rather,olaction-related circuitry, as part o a wider integrated unctionaland structural neuronal network, may have been avored in theevolution o H. sapiensin a social context.

However, olaction, and its contribution to gustation with itslinks to reward (pleasure)23and memory, could also be o evolu-tionary relevance, but at a secondary level27regarding the manipu-lation o ood23,52. Although it has been speculated that early mod-ern humans may have ed on a wider array than Neanderthals53,the role that olaction, gustation or memory and reward might havehad in this context must remain open to speculation. Lieberman27suggested that the effect o higher basicranial exion, approximat-

ing pharynx and olactory epithelium, has enhanced the retronasalcontribution o smell to taste52.

Evolutionary changes at the cribriorm plate and the associatedolactory bulbs11,42and other endocranial parts we report here canimplicate changes to the olactory system that appear unique tomodern humans. It is clear, however, that cognitive unctions areincommensurable even with the most sophisticated measurement obrain impressions in endocranial casts. Tereore, palaeoneurologi-cal interpretation o evolutionary variations in cerebral surace suchas reected in the basal endocranium in unctional terms remainsa challenge3,68,12. Although different regions o the prerontal cor-tex (rontal lobes) have been associated with higher integrative andsocial unctions, (or example, decision making)12,2024, regions othe temporal lobes are traditionally related to visual memory, lan-

guage and to theory o mind24,54,55

. All o them are compatible withhigher olactory unctions44.Our study provides a much needed palaeontological basis52,

which draws neuroscientic attention to urther investigation othese structures. Palaeontological data can indicate when duringhuman evolution such structural changes and putative sets o asso-ciated systems have occurred. We show that specimens attributableto early H. sapiensare within the range o modern congurations othe endocranial base o the brain, thus suggesting a rst appearanceat least approximately 130 kyr ago (or example, Singa)56.

We conclude that the evolution o the base o the brain in highlyencephalized human species produced signicant differences inearly HomoH. neanderthalensisevolutionary trajectory comparedwith those observed in early Homo H. sapiens, at basal rontal

and temporal lobes, the details o which have never shown beore.And surprisingly, although both human species showed increaseat the cribriorm plates and olactory bulbs, the spatial position othese structures within the brain differed signicantly. Increasedcribriorm plates suggests larger olactory bulbs11,3841 in mod-ern humans. Tis does not only t with the relative enlargement omidline anterior cranial oor suggested previously2,27but also elu-cidates why, morphologically and when, chronologically this hap-pened in human evolution.

One likely ramework or the palaeoneurological interpretationo these data points to higher olactory unctions (sensuSavic44) inH. sapiens, because all structures in this evolutionary process shareintimate relations to this sensory modality.

Higher olactory unctions44relate odour reception with sociallyrelevant cognitive processes, or example, subliminally smell-mediated


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modulation o human-specic behavior43,47. Other possible ac-tors may relate to the immunological system46, ear49, kinship orgroup recognition4,43,47) or ood manipulation27,5253and could beamong the implications o these new ndings on the evolution othe basal areas o the human brain.

MethodsLandmarks and digitizing procedure. A set o 158 3-D landmarks and semi-landmarks was digitized by hand on the endocranial surace o the cranial baseon 3-D reconstructions o computed tomography scans. Tese landmarks deneboth structures traditionally measured at the cranial base as well as specicallyendocranial 3-D surace morphology o the base o the rontal and temporal lobes(Supplementary able S1; Supplementary Fig. S1).

Computed tomographic scans o 30 common chimpanzees (P. troglodytesverus) and 75 adult recent humans representing geographic variation rom Arica,Asia and Europe, and 14 ossil Pleistocene humans (able 1) were reconstructedand computer models o their 3-D endocranial suraces were generated in Amira4.1 sofware (Mercury Inc.). Shape data were recorded by landmarks on these 3-Dendocranial suraces. Landmark digitizing error was small, as reported elsewhere16.

Te ossils were also digitized by hand in Amira 4.1. Missing data due totaphonomic actors were careully estimated ollowing standard estimation meth-ods available or semilandmark data57. Missing data estimation was perormed

conservatively using the modern human template (Supplementary Fig. S1) orPS estimation by Morpheus et al.(www.morphometrics.org). Te reconstructedlandmarks were then projected onto 3-D surace models o reconstructed ossilsand edited urther by hand in ViewBox4 (www.dhal.com) and Edgewarp sofware(http://brainmap.stat.washington.edu/edgewarp). Tin-plate splines were usediteratively or minimizing the bending energy between the modern human averageand the ossil during the sliding, re-sliding and re-projection procedure17,57.

Beore statistical analyses landmark data were symmetrized17,57, because insome cases (KNM-ER 3733, KNM-ER 3883) an acceptable correction to sheartaphonomic deormation was obtained57(Fig. 6), and because studying asymmetry(petalia) was not an aim o the study.

Statistical analyses. Principal components analysis in orm space, multivariateregression analyses and mean shape comparisons were perormed using routinesprogrammed by Philipp Gunz and Philipp Mitteroecker17, MorphoJ (www.y-wings.org.uk) and the EVAN-toolbox (www.evan-society.org). During 10,000 per-mutations, group sizes were kept constant but group membership was re-sampled.

Te test assessed the statistical signicance o the obser ved mean Procrustes dis-tance between species means, comparing how ofen mean distances were obtainedequal to or greater than the observed ones due to random group membership.

WaldWolowitz runs58test was perormed using Statistica 8.0 (StatSof Inc.) totest the null hypothesis that cribriorm length measurements were drawn rom thesame sample. It expects the data to be arranged in the same way as the t-test doesor independent samples, but does not make any assumption on normality. It is,thus, a useul test when very small sample sizes preclude using traditional paramet-ric statistics (such as Students t-test). In addition, in small samples, z-adjustmentshave been recommended58.

Visualizations and TPS. Finally, the EVAN toolbox was used or calculation andvisualization o specically located PS in mean shape differences. Tese splinesare registration-independent interpolations between two landmark congurations,and most inormative in their closest vicinity16,17,57.

Splines were used to illustrate hypothesis-related eatures o shape differencesbetween the species means. Several PS-grids were calculated according to the

anatomical hypothesis. Te ACF PS-grid was dened by endocranial regionsclose to landmarks 10, 20, 48, 65, 108 (Supplementary able S1; SupplementaryFig. S1). Te MCF PS-grid was positioned close to lms 16, 26, the anterior poleso the temporal lobes within the greater sphenoid wings (landmarks 11, 16, 21 and26) (Supplementary able S1; Supplementary Fig. S1)26. A vertical PS-grid wascalculated close to landmarks 16 and 26 and the lesser sphenoid wings, to indicatethe anteroposterior variation o the midline base due to evolutionary changes at thecribriorm plate relative to the lateral endocranial anteroposterior shifs. Cribriormshape was urther visualized by local white-coloured PS-grid through its delimitinglandmarks 2, 3, 4, 18 and 19 (Supplementary able S1; Supplementary Fig. S1).

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a b c

Figure 6 | Virtual reconstruction of taphonomic deformations in earlyHomosample.(a) Original endocranial surface of the base of the brain of

KNM-ER 3733 (taphonomic shear, indicated by arrows, causes anatomical

distortion shown by tilted line; (b) reconstructed surface of the same fossil

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view of KNM-ER 3883 showing only minor deformations at the endocranial

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AcknowledgementsEmma Mbua, Fred Spoor, Roberto Macchiarelli, Luca Bondioli, George Kouos, Gerhard

Weber, Philippe Mennecier, Alain Froment, Maria eschler-Nicola, Dan Lieberman,

the NESPOS society (http://www.nespos.org), Paul OHiggins, Jane Monge and P.

Tomas Schoenemann (Open Research Scan Archive-ORSA; http://plum.museum.

upenn.edu/~orsa/Welcome.html ) provided access to data. Chris Stringer is a member

o the Ancient Human Occupation o Britain project, unded by the Leverhulme rust.

Tis research is unded by projects CGL-2009-09013 (Spanish Ministry o Science) and

MRN-C-2005-019564-EVAN (European Union).

Author contributionsM.B. developed the project, designed the study, collected measurements and analysed

data and wrote the paper. A.R. developed the project, and worked on the manuscript.

P.G. post-processed and analysed the landmark data and discussed results. A.P.M.

analysed data and discussed results. G.M., K.H., R.K., C.S., J.H. provided data. All

authors were involved in discussion and comments on the manuscript.

Additional informationSupplementary Informationaccompanies this paper at http://www.nature.com/

naturecommunications

Competing nancial interests:Te authors declare no competing nancial interests.

Reprints and permissioninormation is available online at http://npg.nature.com/

reprintsandpermissions/

How to cite this article:Bastir, M. et al.Evolution o the base o the brain in highly

encephalised human species. Nat. Commun.2:588 doi: 10.1038/ncomms1593 (2011).

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Evolution of the Base of the Brain