Abstract
Compared to their putative insectivore-like ancestors, extant primates show an enlarged brain relative to body weight, a larger neocortex and proportionally decreased olfactory bulbs. Besides hypotheses based on the comparative neuroanatomy of extant taxa, the only direct evidence documenting such long-term evolutionary history is provided by fossil endocasts. However, due to the unpredictable yet unavoidable impact of taphonomic processes, the reliability of data from the fossil record is complicated by the nature of the investigated structures themselves. Nonetheless, palaeoneurology has recently enlarged its traditional investigative toolkit by integrating descriptive morphology with advanced methods of high-resolution 3D imaging and computing. In addition to the development of digital restoration techniques, the introduction of analytical methods for investigating topographic differences in morphostructural organization and quantitatively characterizing intra- and interspecific variation patterns provides new possibilities for the study of the primate fossil record, especially for assessing brain evolutionary tracks.
References
Amunts K, Schleicher A, Bürgel U, Mohlberg H, Uylings HBM, Zilles K (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412:319–341
Armstrong E, Falk D (1982) Primate brain evolution: methods and concepts. Plenum Press, New York
Barton RA (1998) Visual specialization and brain evolution in primates. Proc Biol Sci 265:1933–1937
Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 405:1055–1058
Bayly P, Taber L, Kroenke C (2014) Mechanical forces in cerebral cortical folding: a review of measurements and models. J Mech Behav Biomed Mater 29:568–581
Beaudet A (2015) Caractérisation des Structures Crânio-Dentaires Internes des Cercopithécoïdes et Etude Diachronique de leurs Variations Morphologiques dans la Séquence Plio-Pléistocène Sud-Africaine. PhD dissertation, Université de Toulouse
Beaudet A, Dumoncel J, de Beer F, Duployer B, Durrleman S, Gilissen E, Hoffman J, Tenailleau C, Thackeray JF, Braga J (2016) Morphoarchitectural variation in South African fossil cercopithecoid endocasts. J Hum Evol 101:65–78
Benazzi S, Bookstein FL, Strait DS, Weber GW (2011) A new OH5 reconstruction with an assessment of its uncertainty. J Hum Evol 61:75–88
Brain CK (1981) The hunters of the hunted? An introduction to African cave Taphonomy. University of Chicago Press, Chicago
Bruner E (2004) Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo. J Hum Evol 47:279–303
Bruner E, Mantini S, Ripani M (2009) Landmark-based analysis of the morphological relationship between endocranial shape and traces of the middle meningeal vessels. Anat Rec 292:518–527
Connolly CJ (1950) External morphology of the primate brain. C.C. Thomas, Springfield
de Winter W, Oxnard CE (2001) Evolutionary radiations and convergences in the structural organization of the mammalian brain. Nature 409:710–714
Dumoncel J, Durrleman S, Braga J, Jessel J-P, Subsol G (2014) Landmark-free 3D method for comparison of fossil hominins and hominids based on endocranium and EDJ shapes. Am J Phys Anthropol 153(suppl 56):110 (abstract)
Durrleman S (2010) Statistical models of currents for measuring the variability of anatomical curves, surfaces and their evolution. PhD dissertation, Université Nice-Sophia Antipolis
Durrleman S, Pennec X, Trouvé A, Ayache N, Braga J (2012a) Comparison of the endocranial ontogenies between chimpanzees and bonobos via temporal regression and spatiotemporal registration. J Hum Evol 62:74–88
Durrleman S, Prastawa M, Korenberg JR, Joshi S, Trouvé A, Gerig G (2012b) Topology preserving atlas construction from shape data without correspondence using sparse parameters. In: Ayache N, Delingette H, Golland P, Mori K (eds) MICCAI 2012, Part III. LNCS, vol 7512. Springer, Heidelberg, pp 223–230
Falk D (1981) Sulcal patterns of fossil Theropithecus baboons: phylogenetic and functional implications. Int J Primatol 2:57–69
Falk D (1982) Mapping fossil endocasts. In: Armstrong E, Falk D (eds) Primate brain evolution: methods and concepts. Plenum Publishing Company, New York, pp 217–226
Falk D (2009) The natural endocast of Taung (Australopithecus africanus): insights from the unpublished papers of Raymond Arthur Dart. Am J Phys Anthropol 49:49–65
Falk D (2014) Interpreting sulci on hominin endocasts: old hypotheses and new findings. Front Hum Neurosci 8:134
Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47
Fischl B, Rajendran N, Busa E, Augustinack J, Hinds O, Yeo BT, Mohlberg H, Amunts K, Zilles K (2008) Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex 18:1973–1980
Freedman L (1957) The fossil Cercopithecoidea of South Africa. Ann Transv Mus 23:121–262
Freedman L (1961) New cercopithecoid fossils, including a new species, from Taung, Cape Province, South Africa. Ann S Afr Mus 46:1–14
Freedman L (1976) South African fossil Cercopithecoidea: a re-assessment including a description of new material from Makapansgat, Sterkfontein and Taung. J Hum Evol 5:297–315
Gazin CL (1965) An endocranial cast of the Bridger middle Eocene primate Smilodectes gracilis. Smithson Misc Coll 149:1–14
Gilissen E (2001) Structural symmetries and asymmetries in human and chimpanzee brains. In: Falk D, Gibson KR (eds) Evolutionary anatomy of the primate cerebral cortex. Cambridge University Press, Cambridge, pp 187–215
Glaunès JA, Joshi S (2006) Template estimation from unlabeled point set data and surfaces for computational anatomy. In: Pennec X, Joshi S (eds) Proceedings of the international workshop on the Mathematical Foundations of Computational Anatomy. Copenhagen, pp 29–39
Gómez-Robles A, Hopkins D, Sherwood C (2013) Increased morphological asymmetry, evolvability and plasticity in human brain evolution. Proc R Soc B Biol Sci 280:20130575
Gómez-Robles A, Hopkins D, Sherwood CC (2014) Modular structure facilitates mosaic evolution of the brain in chimpanzees and humans. Nat Comm 5:4469
Gonzales LA, Benefit BR, McCrossin ML, Spoor F (2015) Cerebral complexity preceded enlarged brain size and reduced olfactory bulbs in old world monkeys. Nat Comm 6:7580
Gunz P (2015) Computed tools for paleoneurology. In: Bruner E (ed) Human paleoneurology. Springer, Zurich, pp 39–55
Gunz P, Mitteroecker P, Bookstein, FL, Weber GW (2004) Computer-aided reconstruction of incomplete human crania using statistical and geometrical estimation methods. Enter the past: computer applications and quantitative methods in archaeology. BAR International Series, Oxford, pp 96–98
Gunz P, Mitteroecker P, Neubauer S, Weber GW, Bookstein FL (2009) Principles for the virtual reconstruction of hominin crania. J Hum Evol 57:48–62
Hilgetag CC, Barbas H (2005) Developmental mechanics of the primate cerebral cortex. Anat Embryol 210:411–417
Hill WCO (1972) Evolutionary biology of the primates. Academic, London
Holloway RL (1978) The relevance of endocasts for studying primate brain evolution. In: Noback CR (ed) Sensory systems of primates. Plenum Press, New York, pp 181–200
Holloway RL, Broadfield DC, Yuan MS (2004) The human fossil record: brain endocasts – the paleoneurological evidence. Wiley-Liss, New York
Kaas JH (2002) Convergences in the modular and areal organization of the forebrain of mammals: implications for the reconstruction of forebrain evolution. Brain Behav Evol 59:262–272
Kaas JH (2006) Evolution of the neocortex. Curr Biol 16:910–914
Kobayashi Y, Matsui T, Haizuka Y, Ogihara N, Hirai N, Matsumura G (2014) Cerebral sulci and gyri observed on macaque endocasts. In: Akazawa T, Ogihara N, Tanabe HC, Terashima H (eds) Dynamics of learning in Neanderthals and modern humans, vol 2. Springer, Japan, pp 131–137
Le Gros Clark WE (1971) The antecedents of man: an introduction to the evolution of the primates. Edinburgh University Press, Edinburgh
Le Gros Clark WE, Cooper DM, Zuckerman S (1936) The endocranial cast of the chimpanzee. J Roy Anthropol Inst 66:249–268
Leakey LSB, Tobias PV, Napier JR (1964) A new species of genus Homo from Olduvai Gorge. Nature 202:7–9
Meyer F, Beucher S (1990) Morphological segmentation. J Vis Commun Image Represent 1:21–46
Neubauer S (2014) Endocasts: possibilities and limitations for the interpretation of human brain evolution. Brain Behav Evol 84:117–134
Neubauer S, Gunz P, Hublin J-J (2009) The pattern of endocranial ontogenetic shape changes in humans. J Anat 215:240–255
Neubauer S, Gunz P, Hublin J-J (2010) Endocranial shape changes during growth in chimpanzees and humans: a morphometric analysis of unique and shared aspects. J Hum Evol 59:555–566
Orliac MJ, Ladevèze S, Gingerich PD, Lebrun R, Smith T (2014) Endocranial morphology of Palaeocene Plesiadapis tricuspidens and evolution of the early primate brain. Proc R Soc B 281:20132792
Preuss TM, Goldman-Rakic PS (1991a) Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca. J Comp Neurol 310:429–474
Preuss TM, Goldman-Rakic PS (1991b) Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca. J Comp Neurol 310:475–506
Radinsky L (1967) The oldest primate endocast. Am J Phys Anthropol 27:385–388
Radinsky L (1970) The fossil evidence of prosimian brain evolution. In: Noback CR, Montagna W (eds) Primate brain. Appleton-Century-Croft, New York, pp 209–224
Radinsky L (1973) Aegyptopithecus endocasts: oldest record of a pongid brain. Am J Phys Anthropol 39:239–247
Radinsky L (1974) The fossil evidence of anthropoid brain evolution. Am J Phys Anthropol 41:15–28
Radinsky L (1975) Primate brain evolution. Am Sci 63:656–663
Radinsky L (1982) Some cautionary notes on making inferences about relative brain size. In: Armstrong E, Falk D (eds) Primate brain evolution: methods and concepts. Plenum, New York, pp 29–37
Rakic P, Kornack DR (2001) Neocortical expansion and elaboration during primate evolution: a view from neuroembryology. In: Falk D, Gibson KR (eds) Evolutionary anatomy of the primate cerebral cortex. Cambridge University Press, Cambridge, pp 30–56
Roerdink JBTM, Meijster A (2001) The watershed transform: definitions, algorithms and parallelization strategies. Fund Inform 41:187–228
Rogers J, Kochunov P, Zilles K, Shelledy W, Lancaster J, Thompson P, Duggirala R, Blangero J, Fox PT, Glahn DC (2010) On the genetic architecture of cortical folding and brain volume in primates. NeuroImage 53:1103–1108
Ronan L, Fletcher PC (2015) From genes to folds: a review of cortical gyrification theory. Brain Struct Funct 220:2475–2483
Semendeferi K, Lu A, Schenker N, Damasio H (2002) Humans and great apes share a large frontal cortex. Nat Neurosci 5:272–276
Silcox MT, Benham AE, Bloch JI (2010) Endocasts of Microsyops (Microsyopidae, primates) and the evolution of the brain in primitive primates. J Hum Evol 58:505–521
Specht M, Lebrun R, Zollikofer CPE (2007) Visualizing shape transformation between chimpanzee and human braincases. Vis Comput 23:743–751
Spoor F, Zonneveld F, Macho GA (1993) Linear measurements of cortical bone and dental enamel by computed tomography: applications and problems. Am J Phys Anthropol 91:469–484
Stephan H, Baron G, Frahm HD (1991) Comparative brain research in mammals volume 1. Insectivora. Springer, New York
Subsol G (1995) Construction Automatique d’Atlas Anatomiques Morphométriques à Partir d’Images Médicales Tridimensionnelles. PhD dissertation, Ecole Centrale de Paris
Subsol G (1998) Crest lines for curve based warping. In: Toga A (ed) Brain warping. Academic Press, San Diego, pp 241–262
Subsol G, Gesquière G, Braga J, Thackeray F (2010) 3D automatic methods to segment “virtual” endocasts: state of the art and future directions. Am J Phys Anthropol 141(suppl 50):226–227
Tallinen T, Chung JY, Rousseau F, Girard N, Lefèvre J, Mahadevan L (2016) On the growth and form of cortical convolutions. Nat Phys. doi:10.1038/nphys3632
Tallman M, Amenta N, Delson E, Frost SR, Ghosh D, Klukkert ZS, Morrow A, Sawyer GJ (2014) Evaluation of a new method of fossil retrodeformation by algorithmic symmetrization: crania of papionins (primates, Cercopithecidae) as a test case. PLoS One 9(7):e100833
Toro R (2012) On the possible shapes of the brain. Evol Biol 39:600–612
Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318
von Bonin G, Bailey P (1961) Pattern of the cerebral isocortex. Primatologia II/2. Karger, New York
Weber GW, Bookstein FL (2011) Virtual anthropology: a guide to a new interdisciplinary field. Springer, London
Welker W (1990) Why does cerebral cortex fissure and fold? A review of determinants of gyri and sulci. In: Jones EG, Peters A (eds) Cerebral cortex. Vol 8b. Comparative structure and evolution of cerebral cortex, Part II. Plenum Press, New York, pp 3–136
Yoshizawa S, Belyaev A, Yokota H, Seidel HP (2007) Fast and faithful geometric algorithm for detecting crest lines on meshes. Proceedings of the 15th Pacific conference on computer graphics and applications, pp 231–237
Yoshizawa S, Belyaev A, Yokota H, Seidel HP (2008) Fast, robust, and faithful methods for detecting crest lines on meshes. Comput Aided Geom D 25:545–560
Zilles K, Armstrong E, Schleicher A, Kretschmann HJ (1988) The human pattern of gyrification in the cerebral cortex. Anat Embryol 179:173–179
Zilles K, Kawashima R, Dabringhaus A, Fukuda H, Schormann T (2001) Hemispheric shape of European and Japanese brains: H 3-D MRI analysis of intersubject variability, ethnical, and gender differences. NeuroImage 13:262–271
Zilles K, Palomero-Gallagher N, Amunts K (2013) Development of cortical folding during evolution and ontogeny. Trends Neurosci 36:275–284
Zollikofer CPE (2002) A computational approach to paleoanthropology. Evol Anthropol 11:64–67
Zollikofer CPE, Ponce de León MS (2005) Virtual reconstruction: a primer in computer-assisted paleontology and biomedicine. Wiley Interscience, Hoboken
Zollikofer CPE, Ponce de León MS, Martin RD (1998) Computer-assisted paleoanthropology. Evol Anthropol 6:41–54
Acknowledgements
We are grateful to the editors E. Bruner, N. Ogihara and H. Tanabe for their kind invitation to contribute this volume. We are indebted to J. Cuisin (Paris), G. Fleury (Toulouse), S. Potze (Pretoria), W. Wendelen (Tervuren) and B. Zipfel (Johannesburg) for having granted access to fossil and comparative materials under their care from the Ditsong National Museum of Natural History (Pretoria), the Musée d’Histoire naturelle in Toulouse, the Musée national d’Histoire naturelle (Paris), the Royal Museum for Central Africa (Tervuren) and the University of the Witwatersrand (Johannesburg). We also thank K. Carlson and T. Jashashvili (Johannesburg), G. Clément and M. Garcia-Sanz (Paris), B. Duployer and C. Tenailleau (Toulouse), L. Bam, F. de Beer and J. Hoffman (Pretoria) for microtomographic acquisitions performed at the Accès Scientifique à la Tomographie à Rayons-X (AST-RX) imagery platform set at the Musée national d’Histoire naturelle (Paris), at the French Research Federation FERMaT (Toulouse), at the Palaeosciences Centre of the University of the Witwatersrand (Johannesburg) and at the South African Nuclear Corporation (Pelindaba). For scientific contribution and/or discussion and comments to the results summarized in this study, we are especially grateful to J. Braga (Toulouse), L. Bruxelles (Toulouse), M. Cazenave (Pretoria), E. Delson (New York), J. Dumoncel (Toulouse), S. Durrleman (Paris), D. Ginibriere (Toulouse), J. Heaton (Birmingham), R. Holgate (Pretoria), N. Jablonski (University Park), J.P. Jessel (Toulouse), O. Kullmer (Frankfurt), R. Macchiarelli (Poitiers & Paris), M. Nakatsukasa (Kyoto), L. Pan (Toulouse), G. Subsol (Montpellier), D. Stratford (Johannesburg), J.F. Thackeray (Johannesburg) and C. Zanolli (Toulouse). The French research federation FERMaT (FR3089), the National Research Foundation (NRF) and Department of Science and Technology (DST) of South Africa are acknowledged for providing micro-X-ray tomography laboratory facilities. This work was granted access to the HPC resources of CALMIP supercomputing centre under the allocation 2015-[P1440] attributed to the laboratory AMIS (Toulouse). Research is supported by the Centre of Research and Higher Education (PRES) of Toulouse, the Midi-Pyrénées Region and the French Ministry of Foreign Affairs.
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Beaudet, A., Gilissen, E. (2018). Fossil Primate Endocasts: Perspectives from Advanced Imaging Techniques. In: Bruner, E., Ogihara, N., Tanabe, H. (eds) Digital Endocasts. Replacement of Neanderthals by Modern Humans Series. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56582-6_4
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