ARTICLES

Computer-Assisted PaleoanthropologyCHRISTOPH PETER EDUARD ZOLLIKOFER, MARCIA SILVIA PONCE DE LEON, AND ROBERT DENIS MARTIN

In a pioneering study on the Pithecan-thropus IV cranium, radiologist JanWind laid the foundations of CT-basedanalysis of fossil hominids.1 A majorincentive of his research was to shedlight on fossil inner ear structures. As‘‘parts of the microphones of recordersthat were, in fact, operating during thehominids’ lifetime,’’ these structureswere expected to permit inferencesabout the vocalization of the senders.2

At the same time, Conroy and Van-nier3,4 using a matrix-filled ungulateskull, demonstrated the general feasi-bility of CT-based noninvasive fossilpreparation and emphasized the im-portance of three-dimensional (3D)imaging procedures in recognizingspatial relations between hidden ana-tomical structures. Using fossil-spe-cific CT scanning protocols,5 research-ers then set out to analyze a variety ofanatomical features in different fossilhominid taxa.5–8 In the course of thepast decade, through the increasedavailability of high-resolution medicalscanners and computer graphics con-soles,9 medical imaging methods havebecome well-established in paleoan-thropology. We can now characterizecomputer-assisted paleoanthropologyas a discipline that complements clas-sical methods of physical anthropol-ogy with a set of novel tools in threemajor areas: visualization of hiddenanatomical features, morphometricand biomechanical analysis of skeletalstructures, and computer-assisted re-construction of fragmentary fossils.After giving an overview of the currentstate of the methodology (Fig. 1) wewill discuss the implications and con-clusions that can be drawn from CT-based studies in evolutionary anthro-pology.

CT SCANNING INPALEOANTHROPOLOGY

CT is an X-ray-based imaging tech-nology that has become a standardtool in noninvasive medical diagnosis.A typical medical CT scanner consistsof an X-ray source and a correspond-ing detector array that can be rotatedaround a movable patient table. Ab-sorption data sampled from differentangles around the patient can be inte-grated to yield a cross-sectional im-age. Medical CT scanners work withrelatively low irradiation doses andpermit rapid acquisition of serial cross-sectional image data from extensiveregions of the human body. Althoughthey are tuned to the optical X-raydensity of living tissue, these scannerscan, in principle, also be used for dataacquisition from fossils. A major prob-lem arises here from the high densityvalues found in heavily mineralizedfossil bone, its matrix fillings, and sur-rounding rock. Furthermore, abruptchanges in the density gradients (e.g.,from rock to air) as well as insufficientirradiation doses can generate imageartifacts and thus degrade data reliabil-ity. Within certain limits, however,medical scanners can be adapted tothe density range of fossil material bymodification of the scanning param-eters or recalibration of the device.5

Using these techniques, a within-slicespatial resolution of 0.2 mm and abetween-slice resolution of 1 mm canbe achieved.

CT images essentially representX-ray attenuation plots of cross-sec-tional slices. A wealth of informationcan be derived by directly inspectingstacks of contiguous slice images. Onstandard medical CT consoles, linearand angular measurements can bemade with electronic calipers and rul-ers. However, for many further applica-tions, such as taking area measure-

Paleoanthropologists are confronted by a steadily growing number of fossilspecimens exhibiting diversity in both apparent morphology and state of preserva-tion. Studying this material to answer phylogenetic and functional questions requiresextensive qualitative assessment accompanied by quantitative evaluation of largevolumes of data. Over the past decade, major new developments in both respectshave been made possible through the advent of medical imaging technologies, mostnotably computer tomography (CT), and through concomitant progress in computergraphics technology. In paleoanthropology, these techniques offer noninvasive toolsfor visualization of inaccessible regions of the skeleton, computer-assisted recon-struction of fragmentary fossil specimens, and morphometric or biomechanicalanalysis of data derived from CT images. A series of CT based studies has alreadyyielded new insights into character differences between fossil hominid species.

Christoph P.E. Zollikofer, originally trainedas a zoologist, is a research scientist at theAnthropological Institute and the MultiMe-dia Laboratory, Department of ComputerSciences, University of Zurich. His mainresearch interests are the development ofcomputer-based methods to tackle prob-lems of quantitative comparisons and re-constructions in physical anthropology andsurgical planning.Marcia S. Ponce de Leon is an anthropol-ogy graduate working as a research assis-tant at theAnthropological Institute, Univer-sity of Zurich. Using computer-assistedmethods, she is investigating morphologi-cal changes in fossil and modern homi-noids from infancy to adulthood.Robert D. Martin is Professor and Directorof the Anthropological Institute, Universityof Zurich. His main research interest is incomparative primatology, with an empha-sis on allometric scaling in individual devel-opment and evolution.

Key words: computer tomography, morphom-etry, Neanderthals, stereolithography, virtual re-ality

Evolutionary Anthropology 41

ments or visualizing three-dimensionalstructures, it is necessary to distin-guish different structures such as fos-sil bone, endocranial cavities, and ma-trix fillings. This can be done byapplying automated or interactive im-age segmentation procedures. Becauseeach picture element (pixel) of a CTimage represents the object density at

that location, it is possible to definespecific object regions by determiningall data within a characteristic rangeof densities (Fig. 2). Following thisprinciple, called thresholding, struc-tures exhibiting sufficiently homog-enous density can be extracted andtheir boundaries determined withoutuser interaction. In many instances,

however, user-guided segmentation isessential. For example, due to the lim-ited spatial resolution of the CT scan-ner, densities associated with struc-tures smaller than one pixel or thinnerthan the actual slice thickness arebiased toward lower values. Further,bone structures and surrounding ma-terials such as sediments or plasterfilings often show similar density val-ues. Because insufficient contrast ispresent, thresholding techniques willfail to isolate biologically relevantstructures. However, most features canreadily be distinguished by a humanobserver because our eyes are ex-tremely sensitive to textural differ-ences, such as smoothness or graini-ness, between adjacent structures. Asa general rule, image data segmenta-tion requires a human observer who isthoroughly trained in anatomy. Eventhe most sophisticated data-extractionalgorithms are mere tools that cannotin themselves provide biologicalknowledge. The live anthropologist isstill an essential part of the procedure.

VIRTUAL FOSSILSScanning an average-sized fossil cra-

nium at 1 mm slice intervals yields astack of about 150 cross-sectional im-ages, each consisting of 512 3 512pixels (image width x height). Thisresults in roughly 4 3 107 data pointsper examination. It is hence obviousthat the large volumes of data gener-ated by CT scanners constitute aninformation potential that can only beexhaustively explored with the aid ofcomputer graphics hardware and dedi-cated software tools. Visual inspectionof the entire data volume forms thebasis of any further analysis. In a firststep, the 3D structure of the anatomi-cal features isolated through imagesegmentation procedures is recovered(Fig. 2). Using an imaging work sta-tion, it is possible to visualize andmanipulate these structures. More-over, operating a 3D computer mouseand wearing 3D spectacles, an anthro-pologist can manipulate virtual fossilfragments on a stereo screen and in-spect them from any desired angle.This leads into the realm of virtualreality (VR).

VR denotes a computer-graphicsbased setting in which a user interacts

Figure 1. A general framework for computer-assisted paleoanthropology. Data acquisition withcomputer tomography (CT) yields serial sections that are stored in a database. All subsequentdata processing steps are performed in virtual reality (VR); that is, with graphical representationsof the data, using interactive computer graphics tools. Separation of fossil from matrix is basedon 2D image data segmentation procedures. Preprocessed 2D data are then transformed into3D object representations, which can then be manipulated in various ways on the computerscreen to plan and perform reconstructive and intervention tasks. Once a final model has beengenerated, extensive morphometric analyses can be performed in 2D or 3D, using comparativedata from the database. Rapid prototyping technology such as stereolithography is used tocreate real virtuality (RV) objects, or physical models of computer-generated or computer-modified objects. Stereolithographic replication of fossils is a noninvasive alternative to conven-tional casting techniques. Note the iterative and interconnected character of the procedure asa whole: At any stage, data from ‘‘real’’ reality, VR, and RV can be compared and combinedwith information from the database.

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with graphical representations of realor model objects, using tools and per-forming manipulations and move-ments that emulate physical tools andactions.10 Instances of classical VRapplications are flight simulators andarchitectural walk-throughs. Paleoan-thropological VR applications differfrom such engineering applicationswith respect to both data structuresand user interactions. Whereas engi-neering approaches are based on com-paratively simple geometric modelsconstructed with computer aided de-sign (CAD) procedures, biomedical ap-plications start with preexisting ob-jects such as highly complex andindividualized skeletal parts, fromwhich data must first be acquired us-ing ‘‘reverse engineering’’ methods suchas CT.11 Further, there are scale differ-ences that require different ways ofdealing with virtual objects. In engi-neering applications of VR, users typi-cally pass by or fly through objectslarger than their own size. In a paleo-anthropological setting, a more or lessstationary user deals with several smallobjects, such as fossil fragments, in-specting, modifying, and positioningthem relative to each other on a virtualdesktop.

It is apparent that working in VRhas one salient feature that is of imme-diate practical benefit for paleoanthro-

pological applications. Manual proce-dures are highly invasive. For instance,fossil fragments have to be freed fromsurrounding matrix prior to recon-

struction. By contrast, any manipula-tions in VR are completely noninva-sive. If fossil fragments are embeddedin a matrix it is possible to free themwith the electronic chisel of image

segmentation procedures. It is alsopossible to disassemble and reas-semble fossils that have been recon-structed previously with conventionalmethods. Furthermore, virtual cali-pers and rulers permit contact-freeand highly accurate sampling of awide variety of linear, area, and vol-ume measurements.

FROM VIRTUAL REALITY TO REALVIRTUALITY

VR objects such as fossils preparedand reconstructed on a computer canbe transferred back to physical reality(Fig. 1). As opposed to virtual reality,real virtuality (RV) denotes an environ-ment in which a user interacts withphysical models of 3D objects gener-ated or modified by computer-assistedprocedures.11 Physical objects conveytouch-and-feel information and cantherefore be handled, explored, andassembled under much more realisticconditions than can virtual objects ona computer screen. Currently, the mostaccurate automated replication tech-nology available is laser stereolithogra-phy , an industrial technology origi-nally devised for rapid prototyping(i.e., physical modeling) of CAD-gener-ated parts (Fig. 3). As opposed tomilling technology, in which objectsare carved out of a block of material,

In engineeringapplications of VR, userstypically pass by or flythrough objects largerthan their own size. In apaleoanthropologicalsetting, a more or lessstationary user deals withseveral small objects,such as fossil fragments,inspecting, modifying,and positioning themrelative to each other ona virtual desktop.

Figure 2. Graphical data representation and manipulation (extraction of the labyrinthine cavities from the right temporal bone of the Gibraltar 1Neanderthal skull. (a) CT image data (bar indicates 10 mm) are segmented by discriminating between bone and air according to the localobject density (thresholding), extracting external and internal object boundaries (b, contour lines), and eliminating all but the internal contours ofthe petrosal region (c). Working through a series of adjacent CT slices, the 3D structure of the labyrinthine cavities is recovered; its surface isrepresented by a triangle mesh (d). 3D visualization of consecutive steps a-d (e).

ARTICLES Evolutionary Anthropology 43

stereolithography is an additive pro-cess. Objects are built through con-secutive polymerization of thin layersof a photosensitive liquid resin. (Theprocess resembles that of buildingtopo-graphical models by piling layersof cardboard.) A computer-guided ul-traviolet laser beam traces an outlineand cross-hatches onto the surface ofthe resin, inducing local photopolymer-ization (hardening) according to thedesired object structure. Buildingcross-sections one above the otheryields models of arbitrary topologicalcomplexity. This property makes ste-reolithography an excellent tool forbuilding models of natural objects.For instance, this reverse engineeringprocess can be used to convert back tophysical reality skulls that have beenreconstructed in VR.

Stereolithographic replication of fos-sil specimens is a valuable noninva-sive alternative to traditional moldingand casting techniques. Not only canmodels be produced in one single pro-cess, but there is no loss of qualitythrough repeated copying cycles, asoccurs with a latex or silicon mold. Toprevent deformation or sagging of

parts during production, removablesupporting struts are incorporated intothe model. Once polymerized, stereo-lithographic resins exhibit virtually no

shrinkage. For these reasons, the accu-racy of stereolithographic modelsmatches or even surpasses that of con-ventional casts (Fig. 4). The produc-tion process permits replication ofcavities that are not accessible to physi-cal casting methods. Furthermore,models produced with transparent res-ins have the additional benefit of re-vealing information about the relationbetween internal and external ana-tomical features.

Using the CT Scanner forPaleo-Diagnosis

CT images are used in a steadilygrowing number of studies for qualita-tive and quantitative assessment of theinternal anatomical features of fossilskulls. Even early studies revealed as-tonishing details, such as a dislocatedmalleus in the preserved inner earcavities of the Broken Hill specimenand signs of otospongiosis, a pathologi-cal condition, in the Gibraltar 1 petro-sal region.5 These studies led to identi-fication of a distinct cranial venousoutflow pattern in australopithecines.12

Using mid-sagittal cross-sectionalCT images, several researchers stud-ied basicranial and facial orientationin fossil hominids. An early study onthe OH9 Homo erectus cranium re-vealed the elevated position of the

Figure 3. Laser stereolithography. The movements of PC-guided ultraviolet laser beam aremediated by a set of deflecting mirrors. This beams hardens the liquid surface layer of aphotosensitive resin. Consecutive layers are formed, one above the other, by stepwise down-ward movement of the elevator platform. Model production includes generation of removablesupporting struts, which must be incorporated to prevent sagging of the resin during hardening.Assuming a layer thickness of 0.25 mm, a medium-sized cranium consists of approximately 600layers. Production time is about 20 hours and material costs for one cast are about $200 (U.S.).The production costs for a single copy are approximately $2,000 (U.S.).

Figure 4. Accuracy of stereolithographic replicas and conventional casts. Graphs indicatedeviation in percent of measurements taken on the five original fragments of the Gibraltar 2 skull.N530; measurements range from 10 mm to 150 mm. Boxes and lines and dots indicate 50th 6

25/6 40 percentiles and range, respectively.

44 Evolutionary Anthropology ARTICLES

basicranium in this specimen.6 In arecent comparative analysis of fossiland extant hominids, Ross13 demon-strated that basicranial flexion in Aus-tralopithecus africanus and Homo erec-tus follows the pattern for non-hominid primates, whereas archaicand modern Homo sapiens have moreflexed basicrania.

In the investigation of hominiddental evolution, cross-sectional CTimages offer a rich source of infor-mation. In their analyses of austra-lopithecine dentitions, Conroy and col-leagues 8,14–16 were able to showmarked differences in stages and pat-terns of dental development betweenrobust and gracile forms.

Using the CT Scanner as aMorphometric Tool

Taking linear and angular measure-ments from CT images yields rela-tively robust and reliable results aslong as dimensions are in the range ofcentimeters. In the analysis of dentalstructures, however, significant quanti-tative differences between fossil taxaare to be expected in the millimeterand submillimeter range. Measuringat the resolution limit of CT scannersposes technical problems that requirespecial attention to both the tuning ofthe device and the nature of thescanned object. The accuracy and reli-ability of cross-sectional linear mea-surements derived from CT data havebeen evaluated in detail.5,17–20 Underoptimum conditions, CT-based mea-surements of dental enamel thicknessshow an error range of 0.1 mm, thusmatching the quality of direct mea-surements obtained on physical sec-tions.19

Although the feasibility of takingmeasurements from fossil dentalsamples with a medical CT scannerhas been demonstrated in many cases,morphological and histological stud-ies have so far prevailed in this area.21

Nevertheless, given the particular rel-evance of dental features to the studyof human evolution and consideringthe large sample potentially accessibleto nondestructive analysis, CT tech-nique surely has great potential forfuture investigations in this area. Pres-ent-day industrial micro-CT scannersworking at a slice thickness of 0.1 mmoffer within-slice spatial resolutions

below 0.1 mm, and are thus well suitedto study of the essentially 3D nature ofdental structures such as tooth enamel,which has a fluctuating distribution.

CT-based comparative morphomet-ric analyses of the size and orientationof the semicircular canals have yieldedimportant new insights into characterdifferences between fossil hominidspecies.22,23 Whereas the inner ear mor-phology of australopithecines is ape-like, that of Homo erectus resemblesthe morphology of modern humans inshowing a series of common labyrin-thine features that can be associatedwith upright posture and bipedalismin this genus.22 Within the genusHomo, the case of Neanderthals isparticularly interesting, as in all speci-mens of this taxon analyzed so far the

inner ear morphology deviates in acharacteristic manner from the condi-tion found in modern humans. Basedon these findings, it was possible toidentify an isolated juvenile temporalbone as that of a Neanderthal.23

Functional aspects of fossil morphol-ogy have been explicitly addressed instudies of the mechanical propertiesof the mandibular corpus. CT imageswere used to determine the area andspatial distribution of compact bonein cross-sectional mandibular profiles.Moments of inertia derived from thesedata were used to deduce the strainand stress resistance of the mandibu-lar corpus. Being more indicative thanclassic robusticity indices, these pa-rameters show that australopithecinemandibles, as well as the mandible ofOtavipithecus, were designed to resistelevated torsional stress.24–26

Can Computer Tools Contributeto New Morphometrics?

In classical craniometry, instrumentssuch as rulers, calipers, and cranio-stats are used to obtain morphometricdata that are essentially confined tolinear or angular measurements be-tween landmark configurations. In or-der to permit comparability with previ-ous studies, various innovative CT-based studies of fossils have restrictedanalyses to conventional measure-ments.19,22,23 However, serial CT im-ages inherently contain 3D object infor-mation that is just waiting to beexploited. Further, it is common prac-tice to treat multiple linear measure-ments taken from one object as statis-tically independent variables. From abiological point of view, however, gen-eral interdependence of measurementsis a more realistic assumption. Forinstance, it is readily recognized thatdistances measured between land-marks belong to one common geomet-ric framework. Application of conven-tional multivariate statistics mighttherefore be inappropriate.27,28

Given the complexity of the skeletalstructures analyzed and the relativesimplicity of the available tools, thereis an obvious discrepancy between thetotal morphometric information con-tained in the object and the amount ofquantifiable information that is actu-ally accessible. This is mainly a conse-quence of the fact that the measuringtools are incommensurate with theobjects to be measured. The originalpurpose of instruments such as rulerswas to obtain data from ideal Euclid-ean bodies such as man-made engi-neering parts rather than from or-ganic objects. The fundamentalproblem resides in the task of findingan appropriate frame of reference todefine characteristic measurements.This difficulty cannot be readily over-come, as the information obtained isinextricably intertwined with underly-ing hypotheses about what is consid-ered to be biologically significant.29 Toillustrate this, consider the followingexample: Whereas a sphere can befully characterized by its diameter anda 3D-ellipsoid by the length of its threemain axes, this cannot be done with acranium. Yet in a morphometric studyof cranial dimension, it might be rea-sonable to assume, explicitly or implic-

CT-based comparativemorphometric analysesof the size andorientation of thesemicircular canals haveyielded important newinsights into characterdifferences betweenfossil hominid species.

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itly, that characteristic Euclidean di-mensions of an ellipsoid are in someway representative for a cranium, sothat cranial length, width, and heightare significant dimensions. However,because our knowledge of cranial mor-phogenesis and functional morphol-ogy is scarce, the ‘‘true’’ metrics of acranium remain to be revealed. Fur-ther, because mathematical propertiesdo not necessarily correspond to bio-logical properties, it follows that noteven the most stringent mathematicalmodel can generate biologically mean-ingful interpretations without an un-derlying hypothesis about the biologi-cal significance of the measurements.

Given the above reservations aboutthe distinctions between geometric andbiological relevance, it is evident thatcomputer-assisted tools in themselvescannot provide solutions to the long-lasting problems of morphometry. Nev-ertheless, they can greatly facilitatemorphometric analysis. Recent ap-proaches, known as geometric mor-phometrics, which are based on spe-cific concepts of morphospace, havealready yielded valuable statisticaltools for describing form differencesbetween sets of 3D landmarks (shapespace and thin plate spline analysis28;form space, Euclidean distance matrixanalysis30,31). Despite their impressivedescriptive power, however, landmark-based methods have certain shortcom-ings. Commonly used landmarks,

which are usually regarded as homolo-gous points in comparisons betweenphyletic groups, are not evenly distrib-uted over biological objects and do notconsistently have functional relevance.Regions of the skull with numerous,easily defined landmarks (e.g., the fa-cial region) have been repeatedly sub-jected to detailed quantitative analy-ses,32 whereas regions without a highdensity of landmarks (e.g., the cranial

vault and isolated or fragmentary post-cranial bones) have not been thor-oughly studied, despite their consider-able phylogenetic importance.

Therefore, many recent studies aimat an essentially exploratory approach

to morphometrics, using the com-puter as an instrument visualization.With the aid of special-purpose mor-phometric tools, it is possible to quan-tify and visualize morphological fea-tures that are only qualitativelyaccessible with conventional methods.This is especially important for theanalysis of fragmentary fossil speci-mens because harvesting a greatamount of quantifiable data can greatlyfacilitate evolutionary interpretation.

Using VR models of fossils, morpho-metric characteristics can be deter-mined in one, two, and three dimen-sions. The spatial position of classicallandmarks can be established; inter-landmark distances and angles can bederived. Surface area, object thicknessand volume, and other features thatare easy to define but difficult to mea-sure by conventional means can bedetermined.33 Further, complex param-eters such as the characteristics ofsurface curvature can be evaluated.34

Deformational procedures can be usedto compare homologous morpholo-gies by transforming one object intoanother.28,32 Similar procedures canbe used to simulate growth processes.

Using the Computer toReconstruct Fragmentary Fossils

In an early attempt to reconstructthe endocranial volume of the frag-mentary MLD 37/38 Australopithecus

Commonly usedlandmarks, which areusually regarded ashomologous points incomparisons betweenphyletic groups, are notevenly distributed overbiological objects anddo not consistently havefunctional relevance.

Figure 5. Computerized reconstruction of Gibraltar 1. (a) Decomposition of the original specimen. (b) Reconstruction after part repositioning,correction for distortions, and completion of missing parts. Light gray mirror-imaged parts, white: skull roof morphed from a modern Homo sapiensskull.

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africanus specimen, Conroy and Van-nier12 completed missing portions ofthe endocranial cavity in a series ofcross-sectional images by manual im-age segmentation. Summing up thecontribution of each slice, they ob-tained an estimate of the endocranialvolume that was less than that pro-posed with conventional methods.

The development of VR technologyduring the past decade has led to thedevelopment of a set of specific com-puter tools for fossil reconstructur-ing.11,33,35 Fossil fragments that havebeen CT-scanned independently mustbe merged, assembled, and positionedanatomically appropriate positions toobtain a complete model. Missing partsmust be completed by mirroring exist-ing parts from the opposite side or by

rescaling parts from additional speci-mens. It may be necessary to applyredistortion algorithms to fragmentsthat have been deformed during theprocess of fossilization. Kalvin andcolleagues35 used these methods toreconstruct a composite Homo cra-nium, combining the fossil fragmentsof the Sale and Thomas Quarry speci-mens after scaling them to similarsize.

To meet the requirements of com-puter-assisted paleoanthropology, weset about developing and implement-ing a software toolkit (FoRM-IT: FossilReconstruction and Morphometry In-teractive Toolkit), which comprisescomputer graphics procedures for 3Ddata segmentation, visualization, ma-nipulation, and morphometrics within

one common VR framework.11 We nowreport details of the computer-assistedreconstruction and morphometricanalysis of the two Neanderthal skullsfrom the Forbes’ Quarry36 and Devil’sTower37 sites in Gibraltar.

Gibraltar 1The Forbes’ Quarry (Gibraltar 1)

adult skull is relatively complete, butthe skull roof is missing along with alarge part of the left side of the braincase. It emerged from the 3D recon-struction derived from CT scans thatthe upper jaws had been bent out ofshape and internal structures crushedduring fossilization of the skull. Earlyplaster fillings in these regions pro-tected delicate parts from damage, butmade them inaccessible to direct obser-vation. Furthermore, the skull hadbeen deformed when certain originalfragments had been fitted into place atits rear end. Using computer-assistedtools, it was possible to separate andreposition these parts on the com-puter screen (Fig. 5).

The external aspect of the face wascorrected for distortion. This processwas begun by determining a set oflandmarks located in the anatomicalmid-sagittal plane of the cranium. As-suming that the observed deviationsfrom a common geometric plane werecaused by purely exogenous forces,these landmarks were realigned byapplying a special-purpose algorithmmodeling the concomitant deforma-tion of the whole cranium (M. Bichsel,personal communication). Havingdone this, mirror images from therelatively complete right side were usedto restore missing parts on the leftside. The resulting reconstruction wasthen complete, apart from a region ofthe skull roof. By building in an ap-proximate replacement for the miss-ing bone of the appropriate thickness,it was possible to complete the brain-case. This allowed us to produce arelatively complete endocast and todetermine a fairly precise cranial ca-pacity of 1,230 to 1,250 cc.

Further, it was possible to extractinternal structures such as the parana-sal sinuses and the cavities of the rightbony labyrinth (see Fig. 2). We usedthe latter structure to check consis-tency with hypotheses formulated withrespect to the orientation of the semi-

Figure 6. Computerized re-construction of Gibraltar 2.(a) arrows indicate contactpoints established betweenoriginal fragments (dark)and mirrored components(light). (b) stereolithographiccopies of the original frag-ments and the completehand-painted reconstruc-tion.

a

b

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circular canals relative to externallydefined anatomical planes.38 In fact,both the superior and posterior semi-circular canals form an angle of ap-proximately 45o relative to the sagittalplane.

Gibraltar 2The Devil’s Tower Neanderthal child

skull is represented by five individualfragments: an incomplete mandible,

the fused frontals, the right maxilla,the left parietal, and the right tempo-ral.37 Previous study of the perikymataon an unerupted incisor exposed onthe surface of the maxillary specimenhad previously indicated that this childwas approximately three or four yearsold at the time of death.39

The computer-assisted reconstruc-tion of this skull posed intricate meth-odological problems.33 With the fiveoriginal elements, straightforward and

reliable articulation is possible onlybetween the left parietal and the fusedfrontal bones. To establish additionalregions of anatomical contact, it wasnecessary to complete missing partsthrough mirror-imaging of existingfragments (Fig. 6). After rebuildingthe right mandibular premolars bymirror imaging the existing left teeth,it was possible to establish dental oc-clusion with the upper jaw fragment.At this stage, stereolithographic cop-ies of the jaws were generated to checkthe accuracy of dental occlusion. Thehigh perceptual equivalence providedby the real virtuality models, particu-larly tactile feedback, facilitated accu-rate matching and permitted the re-transfer of positional information tothe VR model. In the next reconstruc-tive step, the semicircular canals ofthe preserved right inner ear cavitiesserved as an anatomical compass toorient the temporal bone along thesagittal plane of the skull, defined byan angle of 45o relative to the planes ofthe superior and posterior semicircu-lar canals.38 The oriented temporalbone and its mirror copy were thenplaced on the mandibular condyles.Finally, the temporoparietal suture be-tween the mirrored temporal and theoriginal parietal bone was used todetermine the anatomically appropri-ate position of the cranial vault bones.

Incomplete bilateral symmetry inskull morphology is a potential prob-lem for reconstructions of missingparts using mirror images. It is likely,of course, that minor departures fromsymmetry will be found, and that theperfect symmetry shown in the recon-struction (Fig. 6) is somewhat ideal-ized. It should be noted, however, thatdepartures from bilateral symmetrywill affect any skull reconstruction, sothis is not a new problem arising withcomputerized approaches.

In order to check the general reliabil-ity of reconstruction of the Neander-thal child skull, including the questionof bilateral symmetry, a parallel recon-struction was conducted using a skull,derived from an archeological site, ofa modern human child of comparabledental age and exhibiting a normaldegree of bilateral asymmetry. Thisskull, which was virtually complete,was subjected to CT scanning. After3D reconstruction on the computerscreen, parts were progressively elimi-

Figure 7. Testing of the accuracy of reconstruction of an archeological specimen from the skullof a modern human child (graveyard of St. Laurentius church, Winterthur, Switzerland, ca.eleventh century): (a) The fragments equivalent to those preserved from the Gibraltar 2Neanderthal child skull (see Fig. 6). (b) The modern skull was reconstructed, following identicalsteps. (c): Morphometric comparisons of the right versus the left side of the original and of thereconstruction versus its original state show that positional errors made during the reconstructionare in the same range as departures from bilateral symmetry. Boxes and lines and dots indicate50th 625/640 percentiles and range, respectively.

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nated, using interactive segmentationtools, until the remaining componentswere equivalent to the fossilized frag-ments of the Neanderthal child skull.The missing parts were then repli-cated by mirror imaging and posi-tioned, following exactly the same pro-cedure used with the fossil skull, togenerate a reconstruction comparableto that for the Neanderthal child.

Comparison of the original modernhuman skull with the reconstructedversion shows that little distortion oc-curred in the process of replicatingmissing parts (Fig. 7). This confirmsthe essential reliability of the recon-struction of the Neanderthal child skull

and incidentally shows that, in thiscase at least, deviation from bilateralsymmetry in general skull architec-ture was not an appreciable problem.Measurements taken on different ver-sions of reconstructions of both theNeanderthal skull and that from H.sapiens suggest that reconstructive er-rors are in the same range as that ofanatomical departures from bilateralsymmetry.

Another advantage of data derivedfrom CT scans is that it is possible tovisualize developing elements of thepermanent dentition (Figs. 8, 9). Inthis case, it is possible to produceimages and, as required, replicas, of

developing permanent incisors, ca-nines, and premolars and of uneruptedmolars in both the lower and upperjaws. One feature that can be seenwith the developing permanent lowerdentition of the Devil’s Tower speci-men, most of which is preserved onboth sides in the original, is consider-able asymmetry in the front teeth.Using conventional radiography, thiscondition had already been identifiedas pathological.37,40 Close inspectionof the 3D reconstruction in this region(Fig. 8a) leads to a more confidentpaleopathological diagnosis. The rightlower permanent incisors are normalin shape but show considerable misori-entation, whereas the bone above the

incisor buds lacks any trace of thealveolus of the right deciduous I2. Theassociated structures indicate bone re-sorption after an injury in early child-hood. It is likely that this traumaticevent also affected development of thepermanent dentition, causing the ob-served distortion of the tooth row un-derneath.

The posterior and basal parts of theGibraltar 2 skull cannot be completedby mirror-imaging of autologous partsbecause no fragments are preservedfrom these regions. However, to assesscranial capacity, we attempted to re-construct missing parts by adjusting acomplete endocast of a modern hu-man skull of an individual of compa-rable age (Fig. 9). To this end, a seriesof landmarks was identified on thepreserved endocranial parts of the Ne-

Although Neanderthalscan generally bedistinguished frommodern humans by a setof autapomorphiccharacters, there is aparticular need for newquantitative datadocumenting charactervariation within andbetween groups.

Figure 8. Isolated developing elements of the permanent dentition of the mandible of theGibraltar 2 Neanderthal child skull (a, b, cf. Fig. 6) and that of a modern human child of slightlyyounger, yet comparable, dental age (c, bar represents 10 mm). Note the malposition of theright second incisor bud in the lower jaw of the Neanderthal child (b, pale arrow) and thecorresponding lack of alveolus in the bone (a, dark arrow). The dentition of this Neanderthalchild appears to be more robust than that in the modern child.

ARTICLES Evolutionary Anthropology 49

anderthal child skull and homologouslandmarks were determined on themodern skull. Applying a 3D mor-phing technique proposed by Book-stein,28 the modern landmark constel-lation was transformed into theNeanderthal constellation. The mod-ern endocranial volume was deformedaccordingly. Different variants of basal-occipital completion were evaluatedto study the influence of minor formvariations on the resulting cranial ca-pacity of 1,370 to 1,420 cc.

The Neanderthal CaseThere is an ongoing, vigorous de-

bate about the evolutionary and func-tional significance of the morphologi-cal differences between Neanderthalsand modern humans, especially withrespect to the question of possiblespeciation events in the recent evolu-tionary history of Homo.41–43 AlthoughNeanderthals can generally be distin-guished from modern humans by a setof autapomorphic characters, 23,33,44,45

there is a particular need for newquantitative data documenting charac-

ter variation within and betweengroups.

It has been long stated that Neander-thals have more robust cranial bonesthan modern humans do, but it hasbeen difficult to quantify this differ-ence. For example, because of theextreme paucity of appropriate land-marks on the braincase, as well aslocal variation in individual overallsize, attempts to quantify cranial vaultbone thickness long remain restrictedto a small number of anatomical loci.46

Computer tools prove especially use-ful in analysis of the fluctuating thick-ness of these bones. Computer-gener-ated thickness maps of the cranialvault bones have revealed complexpatterns of fluctuation (Fig. 10a). It ispossible to compute average thicknessvalues per bone and to relate thesevalues to 2D and 3D morphometricdata. Comparison of juvenile Neander-thals and juvenile modern humansreveals that cranial vault bone thick-ness is elevated relative to both pari-etal surface area and cranial capacity(Fig. 10 b, c). Likewise, in juvenile

Neanderthals the overall robusticity ofthe mandible, measured by the vol-ume of the alveolar corpus, appearselevated in relation to cranial capacity.Computerized 3D representation ofmandibles permits sampling of cross-sectional areas along the dental ar-cade. The resulting profiles are clearlydistinct in Neanderthal and modernchildren (Fig. 10 d, e). Although thesemorphometric differences may have astrong environmental component,46

their appearance at a relatively earlyindividual age23,33,44 suggests distinctgrowth programs, thus supporting theinterpretation that Neanderthals andmodern humans are separate species.

Toward a PaleoanthropologicalData Base

In the course of the procedures de-scribed so far, different types of digitaldata such as CT images, 3D objectdata, and morphometric data havebeen generated. Archiving these datafor a large sample of fossil specimenscreates a digital data base. Ideally,

Figure 9. Comparative morphology of the reconstructed Devil’s Tower Neanderthal skull (left) and that of a modern human child with a dental ageof approximately five years (right). Internal structures are visualized on the left sides of the crania (developing permanent dentition, inner earcavities, and endocranial volumes.) The endocast of the Neanderthal skull was completed by morphing data from the modern skull. In themodern skull, note the absence of a chin and the elongated shape of the cranial vault, as well as the elevated position of the lateral semicircularcanal (seen tangentially) relative to the anterior (upper) and posterior canals of the inner ear of the Neanderthal skull.

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Figure 10. 2D and 3D morphometric characteristics of three juvenile Neanderthals. Open squares: DT, Devil’s Tower; E, Engis 2; RdM, Roc de Marsaland modern H. sapiens of comparable dental age (black circles). (a) Fluctuations in the thickness of the left parietal bones of the modern H.sapiens (same individual as in Fig. 9) and the Devil’s Tower Neanderthal. (b, c) thickness of parietal bone versus both cranial capacity and surfacearea of the bone (dots and bars indicate 50th625 percentiles. Endocranial volumes of the incomplete Neanderthal specimens were evaluated byvolume morphing as shown in Figure 9. c: Volume of the mandibular corpus versus cranial capacity. (d) profile of the cross-sectional area of themandibular corpus (pooled data taking maximum values as 100% for each taxon). (e) I,C, PM, and M are the respective positions of incisors,canine, premolars and molars.

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such a database would be augmentedby contributions from different re-search groups and could be accessedto retrieve information from differentlocalities. Although this endeavorraises questions concerning data stan-dardization, security, and access mo-dalities that have yet to be solved, thepotential benefits are obvious. Com-parative morphometric studies on fos-sil hominids would greatly profit fromlarge samples. Furthermore, attempts

at reconstruction of missing partscould extrapolate missing informationfrom similar specimens in the data-base. The risk of damage to fragileoriginal fossil specimens could be re-duced because any desired action, suchas taking measurements or perform-ing alternative reconstructions, couldbe carried out on the basis of thedigital information already in the database.

A combined biomedical database

would open new perspectives and per-mit comparisons between paleoantro-pological and medical data. For ex-ample, by determining areas ofmuscular attachment on fossil frag-ments and combing this informationwith comparative data from extantapes and humans, it is possible toestimate muscular position andstrength, and to test quantitative hy-potheses in functional morphology.Moreover, morphing soft tissue data

Figure 11. (a) Planning surgical correction of a congenitalmalformation (Apert syndrome) on the computer screen.(b) advancement of the midface and the tip of the chin(light and dark parts), and (c) With a stereolithographicmodel. Computer tools and procedures are similar to thoseused in fossil reconstruction (see Figs. 5, 6).

a

c

b

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extant in apes and humans to fossilskeletal data would help create 3Drobot models of extinct hominids.

Future perspectivesBuilding on what has already been

achieved, computer-aided reconstruc-tion of entire hominid skeletons andsoft tissues (e.g., for Neanderthalskulls) is an obvious next step. Thereare also promising possibilities forvisualizing and replicating 3D modelsof the average condition for individualtaxa such as that of the typical Nean-derthal in contrast with that of Homosapiens, and of hypothetical intermedi-ates between, for example, Homo erec-tus and Neanderthals. Systems of thekind presented here can be used in thefuture for planning and monitoringthe preparation of new specimens, par-ticularly where delicate structures areinvolved. Indeed, it should be possible,at least with some specimens, to ‘‘ex-tract’’ a fossil from its matrix andproduce a reliable replica without pre-paring the fossil itself. In this andother respects, there is great scope forthe production of replicas of differentkinds for both research and teachingpurposes. Effective exploitation of themass of 3D data generated by thesetechniques is still in its infancy, andwill undoubtedly lead to a more pro-found understanding of morphologi-cal differences between taxa. The in-creased availability of quantitative datacan also open new applications for thestudy of biomechanics such as thoseinvolved in mastication and walking.

Overall, however, one of the mostencouraging general perspectives forthe future is the continued develop-ment of positive interaction betweenanthropology and medicine. This isparticularly likely to take place in ar-eas such as surgical planning andsimulation of growth processes. Com-puter-assisted surgical planning andsurgical rehearsal with custom stereo-lithographic models is procedurallysimilar to computer assisted fossil re-construction. Our methodology has sofar been used to provide computerresources as well as stereolithographicreplicas for training complex interven-tions in more than 30 cases47 (Fig. 11).There is enormous potential for 3Dsimulation on the computer screen ofgrowth processes in morphological

structures and the generation of physi-cal replicas, for example of hypotheti-cal intermediate stages. By exploitingall of the possibilities provided by thetransition from virtual reality to realvirtuality, we can move even closer to aproper understanding of real reality.

ACKNOWLEDGMENTSSpecial thanks are due to P. Stucki,

Director of the Multimedia Labora-tory at the University of Zurich, whoseinvaluable support, guidance and col-laboration have accompanied our workfrom the onset. We also thank C.B.Stringer (Paleontology Department ofthe Natural History Museum, Lon-don) for kindly arranging for us toperform CT scans of the GibraltarNeanderthals, as well as for his contin-ued interest and provision of expertadvice on these intriguing hominids.Official permission from the NaturalHistory Museum is gratefully acknowl-edged. We are also much indebted tothe late Professor W.A. Fuchs (Radiol-ogy Department of the Zurich Univer-sity Hospital) for technical supportand to Ciba-Geigy Polymers Division,Marly, for supplying stereolithographicresins. Our research was supported bySwiss NSF grants #31-32360.91 and#31-42419.94 to R.D. Martin and P.Stucki.

REFERENCES1 Wind J (1984) Computerized X-ray tomographyof fossil hominid skulls. Am J Phys Anthropol63:265–282.2 Wind J, Zonneveld FW (1985) Radiology offossil hominid skulls. In Tobias PV (ed), HominidEvolution: Past, Present and Future, pp 437–442.New York: Alan R. Liss.3 Conroy GC, Vannier MW (1984) Noninvasivethree dimensional computer imaging of matrixfilled fossil skulls by high resolution computedtomography. Science 226:457–458.4 Conroy GC, Vannier MW (1985) Endocranialvolume determination of matrix-filled skulls us-ing high-resolution computed tomography. InTobias PV (ed) Hominid Evolution: Past, Presentand Future, pp 419–426. New York: Alan R. Liss.5 Zonneveld FW, Wind J (1985) High-resolutioncomputed tomography of fossil hominid skulls: Anew method and some results. In Tobias PV (ed),Hominid Evolution: Past, Present and Future, pp427–436. New York: Alan R. Liss.6 Maier W, Nkini A (1984) Olduvai hominid 9:New results of investigation. Cour Forsch-InstSenckenberg 69:123–130.7 Conroy GC, Vannier MW (1986) Three-dimen-sional computer imaging: Some anthropologicalapplications. In Else JG, Lee PC (eds), PrimateEvolution, pp 211–222. Cambridge: CambridgeUniversity Press.

8 Conroy GC, Vannier MW (1987) Dental develop-ment of the Taung skull from computerized to-mography. Nature 329:625–627.

9 Vannier MW, Conroy GC (1989) Imaging work-stations for computer-aided primatology: Prom-ises and pitfalls. Folia Primatol 53:7–21.

10 Bresenham J, Jacobs P, Sadler L, Stucki P(1993) Real virtuality: Stereolithography—Rapidprototyping in 3D. Proc SIGGRAPH 93:377–378.11 Zollikofer CPE, Ponce de Leon MS (1995)Tools for rapid prototyping in the biosciences.IEEE CG&A 15:48–55.12 Conroy GC, Vannier MW, Tobias PV (1990)Endocranial features of Australopithecus africa-nus revealed by 2D and 3D computed tomogra-phy. Science 247:838–841.13 Ross CHM (1995) Basicranial flexion, relativebrain size, and facial kyphosis in Homo sapiensand some fossil hominids. Am J Phys Anthropol98:575–593.14 Conroy GC, Vannier MW (1991) Dental devel-opment in South African australopithecines, PartI. Problems of pattern and chronology. Am J PhysAnthrol 86:137–156.16 Conroy GC, Vannier MW (1988) Alleged syn-apomorphy of the M1/I1 eruption pattern inrobust australopithecines and Homo. Evidencefrom high resolution computed tomography. AmJ Phys Anthropol 75:487–492.17 Grine FE (1991) Computed tomography andthe measurement of enamel thickness in extanthominids: Implications for its palaeontologicalapplication. Palaeontol Afr 28:61–69.18 Conroy GC (1991) Enamel thickness in SouthAfrican australopithecines: Noninvasive evalua-tion by computed tomography. Palaeont Afr 28:53–59.19 Spoor CF, Zonneveld FW, Macho GA (1993)Linear measurements of cortical bone and dentalenamel by computed tomography: Applicationsand problems. Am J Phys Anthropol 91:469–484.20 Spoor CF, Zonneveld FW (1995) Morphom-etry of the primate bony labyrinth: A new methodbased on high-resolution computed tomography.J Anat 186:271–286.21 Macho GA, Wood BA (1995) The role of timeand timing in hominid dental evolution. EvolAnthropol 4:17–31.22 Spoor F, Wood B, Zonneveld F (1994) Implica-tions of early hominid labyrinthine morphologyfor evolution of human bipedal locomotion. Na-ture 369:845–848.23 Hublin JJ, Spoor F, Braun M, Zonneveld F,Condemi S, (1996) A late Neanderthal associatedwith Upper Paleolithic artefacts. Nature 381:224–226.24 Daegling DJ (1989) Biomechanics of cross-sectional size and shape in the hominid mandibu-lar corpus. Am J Phys Anthropol 80:91–106.25 Daegling DJ, Grine FE (1991) Compact bonedistribution and biomechanics of early hominidmandibles. Am J Phys Anthropol 86:321.26 Schwartz GT, Conroy GC (1996) Cross-sec-tional geometric properties of the Otavaipithecusmandible. Am J Phys Anthropol 99:613–623.27 Lele S, Richtsmeier JT (1990) Statistical mod-els in morphometrics: Are they realistic? SystZool 39:60–69.28 Bookstein FL (1991) Morphometric Tools forLandmark Data. Cambridge: Cambridge Univer-sity Press.29 Bookstein FL (1994) Can biometrical shape bea homologous character? In Hall BK (ed), Homol-ogy: The Hierarchical Basis of Comparative Biol-ogy, pp 197–227.30 Lele S, Richtsmier JT (1991) Euclidean dis-tance matrix analysis: A coordinate-free ap-proach for comparing biological shapes usinglandmark data. Am J Phys Anthropol 86:415–427.

ARTICLES Evolutionary Anthropology 53

31 Richtsmeier JT, Lele S (1990) Analysis ofcraniofacial growth in Crouzon syndrome usinglandmark data. J Craniofac Gen Dev Biol 10:39–62.

32 Lynch JM, Wood CG, Luboga SA (1996) Geo-metric morphometrics in primatology: Craniofa-cial variation in Homo sapiens and Pan tro-glodytes. Folia Primatol 67:15–39.

33 Zollikofer CPE, Ponce de Leon MS, MartinRD, Stucki P (1995) Neanderthal computer skulls.Nature 375:283–285.

34 Dean D, Gueziec A, Cutting B (1995) Homol-ogy: Selection of landmarks, space curves, andpseudolandmarks in the creation of deformabletemplates. In Mardia KV, Gill CA (eds, Proceed-ings in Current Issues in Statistical Shape Analy-sis, 203–205. Leeds: Leeds University Press.

35 Kalvin AD, Dean D, Hublin J-J (1995) Recon-struction of human fossils. IEEE CG&A 15:12–15.

36 Busk G (1864) On a very ancient humancranium from Gibraltar. Br Assoc Adv Sci1864:91.

37 Garrod DAE, Buxton LHD, Smith GE, BateDMA (1928) Excavation of a Mousterian rock-shelter at Devil’s Tower, Gibraltar. J AnthropolInstit 58:33,196113.

38 Delattre A, Fenart R (1960) L’hominisation ducrane etudiee par la methode vestibulaire. Paris:CNRS.

39 Dean MC, Stringer CB, Bromage TG (1986)Age at death of the Neanderthal child from Devil’sTower, Gibraltar and the implications for studiesof general growth and development in Neander-thals. Am J Phys Anthropol 70:301–309.

40 Skinner MF, Sperber GH (1982) Atlas of Radio-graphs of Early Man. New York: Alan R. Liss.

41 Trinkaus E, Shipman P (1992) The Neander-thals: Changing the Image of Mankind. New York:Knopf.

42 Stringer CB, Gamble C (1993) In Search of theNeanderthals: Solving the Puzzle of Human Ori-gins. London: Thames and Hudson.43 Tattersall I (1995) The Last Neanderthal: TheRise, Success, and Mysterious Extinction of ourClosest Human Relatives. New York: Macmillan.44 Schwartz JH, Tattersall I (1996) Significanceof some previously unrecognized apormorphiesin the nasal region of Homo neanderthalensis.Proc Natl Acad Sci USA 93:10852–10856.45 Heim JL (1997) Ce que nous dit le nez duneanderthalien. La Recherche 294:66–70.46 Liebermann DE (1996) How and why humansgrow thin skulls: Experimental evidence for sys-temic cortical robusticity. Am J Phys Anthropol101:217–236.47 Stucki P, Zollikofer CPE, Sailer HF (1997)Virtual reality and real virtuality in cranio-maxillofacial surgery. J Cranio-maxillofac Surg24:111.

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