Chinese Science Bulletin

© 2008 SCIENCE IN CHINA PRESS ARTICLES Springer

The brain morphology of Liujiang cranium fossil by three-dimensional computed tomography

WU XiuJie1†, LIU Wu1, DONG Wei1, QUE JieMin2 & WANG YanFang2

1 Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China; 2 Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China The Liujiang cranium is the most complete and well-preserved late fossils ever unearthed in south China. Because the endocranial cavity is filled with hard stone matrix, earlier stud- ies focused only on the exterior morphology of the specimen using the traditional methods. In order to derive more information for the phyletic evaluation of the Liujiang cranium, high-resolution industrial computed tomography (CT) was used to scan the fossil, and the three-dimensional (3D) brain image was reconstructed. Compared with the endocasts of the hominin fossils (Hexian, Zhoukoudian, KNM-WT 15000, Sm 3, Kabwe, Brunn 3, Predmost) and modern Chinese, most morphological features of the Liujiang brain are in common with modern , including a round brain shape, bulged and wide frontal lobes, an enlarged brain height, a full orbital margin and long parietal lobes. A few differ- ences exist between Liujiang and the modern Chinese in our sample, including a strong posterior pro- jection of the occipital lobes, and a reduced cerebellar lobe. The measurement of the virtual endocast shows that the endocranial capacity of Liujiang is 1567 cc, which is in the range of Late Homo sapiens and much beyond the mean of modern humans. The brain morphology of Liujiang is assigned to Late Homo sapiens.

Homo, Liujiang, computed tomography, endocranial capacity, brain evolution

Brain evolution is one of the most important aspects of methods limited the study of human brain evolution. human evolution. The study of brain evolution facilitates Recently, three-dimensional (3D) visualization computer a more comprehensive understanding of human evolu- techniques have been applied to fossil specimens. Com-

tion, phylogeny, language, and intelligence. The most puted Tomography (CT) can explore vertebrate fossils in GEOLOGY direct evidence for the studies of human brain evolution a noninvasive way by transforming a real fossil into a is endocasts (endocranial casts). The endocast is the im- virtual object. High-resolution CT scans can identify the pression taken from the inside of a cranium that retains density difference between the cranial cavities and the the surface features of the brain. By analysis of the brain bone, and make it possible for paleoanthropologists to length, breadth, height and sulcul patterns, we can get extend the study of fossil specimens from the exterior to inferences on brain morphological features and ana- the interior. CT and virtual imaging have facilitated the tomical structure of the fossil hominids[1]. Because developments in paleoneurology. hominin fossils are very rare, it is impossible to really Received October 29, 2007; accepted May 12, 2008 dissect a precious fossil specimen for anatomical studies. doi: 10.1007/s11434-008-0263-z Additionally, since most hominin fossils are incomplete, †Corresponding author (email: [email protected]) Supported by the Knowledge Innovation Program of the Chinese Academy of Sci- or filled with a heavy calcified matrix, it is difficult or ences (Grant No. KZCX2-YW-106), the National Natural Science Foundation of often impossible to reconstruct the endocast in a real China (Grant No. 40772018), the Major Basic Research Projects (Grant No. 2006CB806400) and the International Cooperation Program of MST of China (Grant fossil without destroying it. Accordingly, traditional No. 2007DFB20330) www.scichina.com | csb.scichina.com | www.springerlink.com Chinese Science Bulletin | August 2008 | vol. 53 | no. 16 | 2513-2519

In 1983, CT scanning was applied for the first time to think that the age of Liujiang is probably older, and the hominin fossils by Conroy and Vannier[2]. The partial fossils date back to 101 ka, but more likely to 153 ka. cranium of Australopithecine MLD 37/38 is filled with Alternatively, they would be older than 220 ka[21,22]. stone matrix, and the frontal part of the endocranium In this paper, we used high-resolution industrial CT to and most of the face are missing. Physical reconstruction scan the Liujiang cranium, and reconstruct the 3D brain was impossible to reveal the hidden structures without image. Our goal was to study the interior of the fossil destroying the fossil. Based on the CT scan, the missing specimen, in order to get more information for the cerebrum was restored by drawing and a virtual endo- phyletic evaluation of the Liujiang hominin fossil. cast was reconstructed. The cranial capacity of 425 cc for MLD 37/38 was calculated by virtual tools[3]. Later, 1 Materials and methods the virtual endocasts of STS 5, STS 71, OH 5, GLL 33, 1.1 Materials SK 48, TAUNG 1, BODO, OH 9, NDUTU and Table 1 is the catalogue of endocasts for comparison STEINHEIM were created with the methods of com- ― with Liujiang used in this study. Liujiang, the endocasts puter-assisted paleoanthropology[4 8]. In 2005, Falk et al. of Hexian, ZKD II, ZKD III, ZKD X, ZKD XI, ZKD reconstructed the virtual endocast of “Homo floresien- XII, Kabwe, Brunn 3, Predmost 3, Predmost 4, Predmost sis” (18 ka), which was found on the Indonesian island 9, Predmost 10 and modern Chinese are from the collec- of Flores. The of H. floresiensis is very small, tions of the Institute of Vertebrate Paleontology and Pa- but its endocast shape and the sulcus resemble that of H. leoanthropology, Chinese Academy of Sciences. Our erectus, which are consistent with higher cognitive observations and metric data of KNM-WT 15000 and processing. It indicates that H. floresiensis type speci- Sm 3 are derived from published studies[23―25]. men is not a microcephalic or pygmy[9].

In the 1990s, CT was applied on vertebrate paleon- Table 1 Endocasts for comparison with Liujiang used in the study [10―13] tological materials and dinosaur eggs in China . Endocast Geographic origin Date (ka) [23] Only a few rather complete human skulls have been KNM-WT 15000 Africa 1530 [26] found in China, such as Zhoukoudian (“ZKD”), Dali, Sm 3 Indonesia >1000 [27] Jinniushan, and Liujiang, but studies have primarily fo- Hexian China 412 [28] cused on the exterior morphology of the crania. There ZKD II China 423 [28] has been a paucity of paleoneurological studies in China, ZKD III China 585 [28] and even fewer studies used CT. In 2004, Li et al., col- ZKD X China 423 [28] laborating with French scientists, scanned the Yunxian II ZKD XI China 423 [28] fossil cranium[14]. Because the primary goal was the re- ZKD XII China 423 [25] Kabwe Africa 250 construction and repairing of the distorted skull, the [25] Brunn 3 Europe 26 brain morphology did not show clearly. [25] Predmost 3 Europe 26 The Liujing fossil skull was found in Tongtianyan [25] Predmost 4 Europe 26 Cave of Liuzhou district, Guangxi Zhuang Autonomous [25] Predmost 9 Europe 26 [25] Region. Because the endocranial cavity is filled with Predmost 10 Europe 26 hard stone matrix, earlier studies were only restricted to Modern Chinese (N=31) China Modern the exterior morphology of the skull[15―18]. The exact layer that yielded the fossils is unclear, arguments about 1.2 Virtually reconstructing Liujiang cranium with the chronology have existed for a long time[19―22]. Some CT scans people suggested that the Liujiang hominin remains The Liujiang cranium was scanned in coronal orienta- [20] were rather late, dating back to 68―40 ka . Compared tion by use of the high-resolution industrial CT scans with the Upper cave specimens, the morphological (type: GY-1-450 XCT) housed in the Institute of High characters of the Liujiang cranium and the body shape Energy Physics, Chinese Academy of Sciences. CT scan are more modern. The cranial morphology of Liujiang is parameters were: X-ray tube voltage 430 kV, X-ray tube very close to those of modern Chinese and very few dif- current 9 mA, 0.5-mm slice thickness, every slice expo- ferences exist between them[17―19]. Other researchers sure time 2 minutes. Three hundred slices were scanned

2514 WU XiuJie et al. Chinese Science Bulletin | August 2008 | vol. 53 | no. 16 | 2513-2519 Following recent hominin endocast studies essing software (Amira 4.1) forvolumetric estimations. image-proc- an into loaded were images scanned The cipal componentanalyses 1.3 Measurement of the vi cast. reconstruction ofthe Liujiang cranium and brain endo- the bone and the soil matrix. Figure 2is the3Dvirtual of is theboundary line The black cranium. Liujiang the WU Figure 3 tasks. three-dimensional object Then image data are transf tools. The fossil wasseparated from theinterior matrix. in a virtual reality through interactive computer graphics defined manually were sediment the and tween bone the (www.mc.com/tgs). The boundary of each 2D slice be- data, running Amira (Version 4.1) software by Mercury reconstructions werecreated bypost processing the CT 3D the Workstation, Graphics mm.OnaDell 0.276376 slice is 283 mm, andeach pixel size is0.276367 mm × color depth is 8 bits. The reconstruction diameter ofeach The complete set of slice pixel matrix is 1024×1024, and High Energy Physics,Chinese Academy ofSciences. 2D reconstruction software made by the Institute of The primary scanned slice data were processed with the altogether, and 297 slices of (IB-IL); 9, occipital breadth (OB-OB). breadth occipital (IB-IL); 9, (IEU-IEU); 3, height(PH-CI); 4, breadth frontal (FB-FB); 5, cere mostTI,the the frontal ventral lobe; l pointofthetemporal trusion pointof thefrontal lobe;OB,the thegreat of thelambdoidalIEU, andsagittalsuturesontheinsideofbraincase; most ofthe occipita posteriorprotuberance used in the study. Theeleven landmarks areFP, OP, IB, urements. Figure3isthe landmarksmeasurements and meas- standardized nine and landmarks eleven chose Figure 1 is the image segmentation of a 2D slice of

The landmarks and measurements used in the study (cited from Wu et al Wu et measurements study(citedfrom and Thelandmarks usedinthe XiuJie and perform reconstructive

CTimage wereobtained. rtual endocast and prin- rtual endocastandprin- ormed subsequently into greatest lateral pointoftheoccipitallobe lateral greatest etal. Chinese ScienceBulletin l lobe;IB,theintersectionof coronal andsagittalsuturesonthe insideofth [ 9,23,24,29] obe; CI, the most the obe; CI, ventral pointof thecerebellarhemisphere. 1, bral height(PH-TI); 6, frontal , we | 16| | no. August 2008|vol.53

(showing thesediment matrix insidethecranium). Figure 1 lobe; FI, the most; PH,thehighestpointof parietal the lobe;FI, st; FB, the greatest lateral pro- lateral protrusionpointoftheendocast;FB,greatest est lateral Figure 2 [ 29] ). FP,most anteriorprotuberance The ofthefrontal lobe;OP, the Image segmentation of a 2D slice of the Liujiang cranium segmentation of theLiujiangcranium Image a 2Dsliceof 3Dvirtual image oftheLiujiang cranium andendocast. height(IB-FI); 7, frontal cho 2513-2519 e braincase; IL, theintersection e braincase;IL,

rd (IB-FP); 8, parietal chord Length (FP-OP);Length breadth 2,

ventral pointof

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IL, IEU, FB, OB, PH, FI, TI, CI. The nine measurements two-thirds of the way from the occipital poles. The pa- are length, breadth, height, frontal breadth, cerebral rietal lobes are round, and have no sagittal keel along the height, frontal height, frontal chord, parietal chord and center suture. The frontal lobes are wide, and the orbital occipital breadth. With Amira software, we obtained 9 margin is full. The area of the inferior frontal gyrus is morphometric data of the virtual endocast. According to slightly larger and more prominent on the left side than the landmarks and measurements in Figure 3, the endo- on the right (Figure 4b, c). Lateral view (Figure 4d, e), casts in Table 1 were measured with sliding and spread- the vertex of the endocast is located one-third of the way ing calipers and recorded to the nearest 0.1mm. Each from the centro-parietal lobe. The temporal region is endocast was measured three times and the average was wide. When the endocast is viewed posterior (Figure 4f), used as the final measurement. We performed principal the occipital lobe forms a semi-circular shape, and the component analyses (PCA) using SPSS (version 11.0) to occipital poles are especially prominent. The cerebella look at the interactions among variables. structures are tight and low. Liujiang has more morphological features in common 2 The Liujiang brain morphology with modern humans, and only a few primitive charac- ters were reserved. Compared with modern humans, In the process of human evolution, the brain morphology Liujiang has a bigger and more posterior location of oc- changed. The brain height changed the most, followed cipital lobes, and a steady reduction of cerebella struc- by length and breadth in that order respectively[30]. The tures. These two features are expressed on the endocasts brain of is different from modern humans, of Chinese Homo erectus (eg. Hexian, ZKD III, ZKD X, including a low maximum height, a strong posterior ZKD XI, ZKD XII), African archaic Homo sapiens projection of the occipital lobes, a more anterior position Kabwe and Late Homo Sapiens of Brunn 3, Predomost 3, of the cerebellar lobes relative to the occipital lobes, a Predomost 4, Predomost 9 and Predomost 10. On the flat surface on the frontal lobes, and a short parietal comparative modern Chinese in our sample, the occipi- length. With an enlarged brain, the brain tends to be tall, tal lobes display a steady reduction in volume, and the the frontal lobes tend to be round and broad, the parietal cerebellum are globular. lobes tend to be wide and long, the general shape of the [31,32] brain tends to be round . Figure 4 is the virtual en- 3 The Liujiang cranial capacity docast of Liujiang fossil cranium by CT scan. The Liu- jiang endocast is short and wide with an ovoid form in With Amira Software, the solid matrix contained in the superior view (Figure 4a). The widest point is situated endocranium was removed and the virtual endocast of

Figure 4 Extracted virtual endocast of the Liujiang cranium. a, Superior view; b, basal view; c, anterior view; d, right lateral view; e, left lateral view; f, posterior view.

2516 WU XiuJie et al. Chinese Science Bulletin | August 2008 | vol. 53 | no. 16 | 2513-2519 WU Table 2 SmHex- 3, 15000, KNM-WT Liujiang, on data Metric 4 Metrical comparisons (adapted from Figure 5 poff ing from 1140 to 1600 cc. Adapted from Lee and Wol- erage capacity of 1390 cc for 93 modern Chinese, rang- of the conventional millet seed method, we getthe av- jiang is1567segmentation ccby of CTdata.means By Liujiang was reconstructed. The cranial capacity ofLiu- whose geologicalageisyounger than100ka. our sample, and in the range of the Late men ismuch bigger than th indicates that thecranial capacity ofthe Liujiang speci- among Pleistocene hominins were drawn (Figure 5). It Predmost Predmost 4 Kabwe 3 ZKD ZKD ZKD XII ZKD III XI X Modern Chinese Predmost 9 Brunn 3 ZKD Hexian II KNM-WT Liujiang 15000 Predmost 10 Sm 3

[ 34] Comparison oftheendocastmeasurements among theLiu Cranial capacity and geological age for the Liujiang specimen theLiujiang specimen capacityandgeological agefor Cranial , abivariate plot of cranial capacities and dates Length

Lee andWolpoff 159.8―177.0117.0 ―137.3 119.8―135.2 175.1 151.1 161.1 158.0 116.0 167.9 166.1 173.6 186.9 188.0 175.5 178.1 192.0 146.1 173.5 158.9 156.1

[ 34] ). XiuJie e average modern Chinese in

Breadth

131.0 123.9 113.6 117.0 126.9 128.0 127.1 140.2 130.2 142.1 126.1 136.1 125.3 140.1 124.2 138.5 115.5 120.4 134.2 98.8 100.6 etal. Chinese ScienceBulletin Height 103.0 105.3 100.0 107.0 104.5 114.1 106.2 103.2 132.9 129.0 Homo Sapiens Homo

110.9―133.8 Cerebral in,ohrhmnnfsisadmdr uas(nm) jiang, other hominin fossilsandmodern humans (in mm) height 122.0 105.7 101.3 104.5 119.4 108.1 129.9 124.1 127.9 117.9 112.2 99.2

| 16| | no. August 2008|vol.53

102.9―122.5 h ijagfsi rnu svr utbet dniyn the Liujiang fossil craniumis very suitable to identifying 5 Discussion and conclusion modern Chineseinoursample. Predmost 3,Predmost 4,Predmost 9,Predmost 10and Sapiens Predmost 9, Predmost 10 and African archaic the late height and frontal height. For PC1,Liujiang is close to the variance, and is mainly related to the height, cerebral s and occipitalThe breadth. ances, and is mainly related to the breadth, frontal chord total variance. Thefirst PC explains 63.8%of the vari- 6). The first two components account for 80.5% of the hominin fossils and modern human’s endocasts (Figure information ontheoverall shapeof Chinese.ern Theprincipal componentanalysis provides chord, and occipital chord were inthe range of the mod- cerebral height, frontal breadth, frontal height, parietal 3, Predmost 4, Predmost 9, Predmost 10). The height, the range of the late Homo Sapiens (Brunn 3, Predmost close to the upper limit of the modern Chinese, and in breadth and frontal chord for the Liujiang fossil are mans in our sample are included in Table 2. The length, ian, ZKD, Kabwe, Brunn 3, Predmost and modern hu- breadth Frontal 105.5 107 106.2 100.2 126.1 118.0 123.3 124.8 108.0 115.2 105.9 (1) Thehigh-resolution industrial CT scans used in 93.3 73.1 94.2 99.1 86.0 Kabwe. ForPC 2, Liujiang is close to Brunn 3, Homo Sapiens Homo 86.1―99.9 Frontal 102.1 108.9 101.2 height 93.0 78.2 74.9 68 83.5 86.9 77.0 78.2 79.9 85.6 66.0 95.5 98.3 88.1 94.5 75.1 Brunn 3, Predmost 3, Predmost 4, 69.2―89.097.9 ―114.1 2513-2519 Frontal chord 84.1 104.9 73 79. 91.9 122.2 73.0 85.5 109.5 88.2 118.0 77.6 103.9 89.1 107.1 69.8 econd PC explains 16.7% of of 16.7% PC explains econd 0 86.9

Parietal

116.5 120.3 chord the Liujiang, other 94.5 92.1 95.2 95.5 87.2 93.3 82.9 87.5 93.5 93.0 103.0 92.2 91.5―107.5 Occipital breadth 103.1 117.2 114.0 107.1 110.9 101.9 89.9 95.6 96.6 Homo Homo 2517

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brain size of 600―1251 cc. Archaic Homo sapiens (250―40 ka) has a cranial capacity range between 1100―1500 cc. The cranial capacity of anatomically modern Homo sapiens (40―10 ka) is between 1300― 1750 cc[35,36]. The average capacity of modern Chinese in our sample is 1390 cc, ranging from 1140 to 1600 cc. The cranial capacity of Liujiang is much bigger than the average of modern Chinese in our sample, and in the range of the Late Homo Sapiens. (3) Most morphological features of the Liujiang brain are in common with modern humans, including a round brain shape, an enlarged brain height, bulged and wide frontal lobes, a full orbital margin, and long parietal lobes. However, the Liujiang brain reserved a few primitive characters. Compared with modern humans,

Figure 6 PCA of the morphological data of the Liujiang, other hominin Liujiang has a bigger and more posterior location of oc- fossils and modern Chinese endocasts. cipital lobes, a steady reduction of cerebella structures.

It suggests that Liujiang has a developed primary visual the density differences between bone, air and sediment. It can accurately display the internal anatomical details cortex. In some degree, the development of the Liujiang and allows the reconstruction of the 3D virtual brain brain is primitive. endocast. CT and virtual imaging facilitates more de- (4) Compared with endocasts of KNM-WT 15000, tailed studies in paleoneurology, and makes it possible Sm 3, Hexian, ZKD, Kabwe, Brunn 3, Predmost 3, for paleoanthropologists to extend the study from the Predmost 4, Predmost 9, Predmost 10 and modern Chi- nese in our sample, the morphometric features of the exterior to the interior of the hominin fossils. (2) The cranial capacity of Liujiang is 1567 cc by CT. Liujiang brain are more closely related to Late Homo The brain size increase is one of the most important fea- Sapiens. tures during human evolution. The brain size of Austra- We are indebted to the Mercury (www.mc.com/tgs) for supplying 3D visu- lopithecus (4.4―1.0 Ma) is between 400―500 cc. The alizing software Amira (Evaluation Version). We would like to thank ― Professor Zhang Wending, who gave us many helps in reconstruction of cranial capacity of Homo habilis (2.5 1.6 Ma) ranges the Liujiang endocast. We would extend our special thanks to Dr. Chris- from 510 to 725 cc. Homo erectus (1.7―0.2 Ma) has a topher Norton and Steven Wang for their help in improving the paper.

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