What do brain endocasts tell us? A comparative analysis of the accuracy of sulcal identification by experts and perspectives in palaeoanthropology.
brain endocast
brain evolution
palaeoneurology
sulcal identification
Journal
Journal of anatomy
ISSN: 1469-7580
Titre abrégé: J Anat
Pays: England
ID NLM: 0137162
Informations de publication
Date de publication:
07 Nov 2023
07 Nov 2023
Historique:
revised:
12
10
2023
received:
02
06
2023
accepted:
12
10
2023
medline:
8
11
2023
pubmed:
8
11
2023
entrez:
7
11
2023
Statut:
aheadofprint
Résumé
Palaeoneurology is a complex field as the object of study, the brain, does not fossilize. Studies rely therefore on the (brain) endocranial cast (often named endocast), the only available and reliable proxy for brain shape, size and details of surface. However, researchers debate whether or not specific marks found on endocasts correspond reliably to particular sulci and/or gyri of the brain that were imprinted in the braincase. The aim of this study is to measure the accuracy of sulcal identification through an experiment that reproduces the conditions that palaeoneurologists face when working with hominin endocasts. We asked 14 experts to manually identify well-known foldings in a proxy endocast that was obtained from an MRI of an actual in vivo Homo sapiens head. We observe clear differences in the results when comparing the non-corrected labels (the original labels proposed by each expert) with the corrected labels. This result illustrates that trying to reconstruct a sulcus following the very general known shape/position in the literature or from a mean specimen may induce a bias when looking at an endocast and trying to follow the marks observed there. We also observe that the identification of sulci appears to be better in the lower part of the endocast compared to the upper part. The results concerning specific anatomical traits have implications for highly debated topics in palaeoanthropology. Endocranial description of fossil specimens should in the future consider the variation in position and shape of sulci in addition to using models of mean brain shape. Moreover, it is clear from this study that researchers can perceive sulcal imprints with reasonably high accuracy, but their correct identification and labelling remains a challenge, particularly when dealing with extinct species for which we lack direct knowledge of the brain.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-20-CE27-0009
Informations de copyright
© 2023 The Authors. Journal of Anatomy published by John Wiley & Sons Ltd on behalf of Anatomical Society.
Références
Balzeau, A., Grimaud-Hervé, D. & Jacob, T. (2005) Internal cranial features of the Mojokerto child fossil (East Java, Indonesia). Journal of Human Evolution, 48, 535-553.
Balzeau, A., Holloway, R.L. & Grimaud-Hervé, D. (2012) Variations and asymmetries in regional brain surface in the genus Homo. Journal of Human Evolution, 62(6), 696-706. Available from: https://doi.org/10.1016/j.jhevol.2012.03.007
Balzeau, A. & Mangin, J.F. (2021) Which synergies between paleoanthropology and brain imaging? Symmetry, 13, sym13101974.
Beaudet, A., Holloway, R.L. & Benazzi, S. (2021) A comparative study of the endocasts of OH 5 and SK 1585: implications for the paleoneurology of eastern and southern African Paranthropus. Journal of Human Evolution, 156, 103010. Available from: https://doi.org/10.1016/j.jhevol.2021.103010
Bruner, E. (2019) Human paleoneurology: shaping cortical evolution in fossil hominids. The Journal of Comparative Neurology, 527, 1753-1765.
Bruner, E., Amano, H., de la Cuétara, J.M. & Ogihara, N. (2015) The brain and the braincase: a spatial analysis on the midsagittal profile in adult humans. Journal of Anatomy, 227, 268-276.
Bruner, E. & Beaudet, A. (2023) The brain of Homo habilis: three decades of paleoneurology. Journal of Human Evolution, 174, 103281.
Cofran, Z., Hurst, S., Beaudet, A. & Zipfel, B. (2023) An overlooked Australopithecus brain endocast from Makapansgat, South Africa. Journal of Human Evolution, 178, 103346.
Cointepas, Y., Mangin, J.-F., Garnero, L., Poline, J.-B. & Benali, H. (2001) BrainVISA: software platform for visualization and analysis of multi-modality brain data. NeuroImage, 13, 98.
Connolly, J.C. (1950) External morphology of the primate brain. Springfield, IL: C. C. Thomas.
Corouge, I., Gouttard, S. & Gerig, G. (2004) Towards a shape model of white matter fiber bundles using diffusion tensor MRI, in: 2004 2nd IEEE International Symposium on Biomedical Imaging: Macro to Nano (IEEE Cat No. 04EX821). In: Presented at the 2004 2nd IEEE International Symposium on Biomedical Imaging: Macro to Nano, IEEE, Arlington, VA, USA, pp. 344-347. Arlington, VA: Institute of Electrical and Electronics Engineers. Available from: https://doi.org/10.1109/ISBI.2004.1398545
Davatzikos, C. & Bryan, R.N. (2002) Morphometric analysis of cortical sulci using parametric ribbons: a study of the central sulcus. Journal of Computer Assisted Tomography, 26, 298-307. Available from: https://doi.org/10.1097/00004728-200203000-00024
de Jager, E.J., Risser, L., Mescam, M., Fonta, C. & Beaudet, A. (2022) Sulci 3D mapping from human cranial endocasts: a powerful tool to study hominin brain evolution. Human Brain Mapping, 43, 4433-4443. Available from: https://doi.org/10.1002/hbm.25964
de Jager, E.J., van Schoor, A.N., Hoffman, J.W., Oettlé, A.C., Fonta, C., Mescam, M. et al. (2019) Sulcal pattern variation in extant human endocasts. Journal of Anatomy, 235(4), 803-810. Available from: https://doi.org/10.1111/joa.13030
de Vareille, H., Rivière, D., Sun, Z.-Y., Fischer, C., Leroy, F., Neumane, S. et al. (2022) Shape variability of the central sulcus in the developing brain: a longitudinal descriptive and predictive study in preterm infants. NeuroImage, 251, 118837.
Dumoncel, J., Subsol, G., Durrleman, S., Bertrand, A., de Jager, E., Oettlé, A.C. et al. (2021) Are endocasts reliable proxies for brains? A 3D quantitative comparison of the extant human brain and endocast. Journal of Anatomy, 238, 480-488. Available from: https://doi.org/10.1111/joa.13318
Eichert, N., Watkins, K.E., Mars, R.B. & Petrides, M. (2021) Morphological and functional variability in central and subcentral motor cortex of the human brain. Brain Structure & Function, 226, 263-279. Available from: https://doi.org/10.1007/s00429-020-02180-w
Falk, D. (1980) Hominid brain evolution: the approach from paleoneurology. Yearbook of Physical Anthropology, 23, 93-107.
Falk, D. (2014) Interpreting sulci on hominin endocasts: old hypotheses and new findings. Frontiers in Human Neuroscience, 8, 134.
Falk, D., Zollikofer, C.P.E., Ponce de León, M., Semendeferi, K., Alatorre Warren, J.L. & Hopkins, W.D. (2018) Identification of in vivo sulci on the external surface of eight adult chimpanzee brains: implications for interpreting early hominin endocasts. Brain, Behavior and Evolution, 91(1), 45-58.
Fischer, C., Operto, G., Laguitton, S., Perrot, M., Denghien, I. & Rivière, D. (2012) Morphologist 2012: the new morphological pipeline of BrainVISA. In: Presented at the Proceedings of the 18th HBM Scientific Meeting, Neuroimage, Beijing, China. Minnessota: Organization for Human Brain Mapping.
Fournier, M., Combès, B., Roberts, N., Braga, J. & Prima, S. (2011) Mapping the distance between the brain and the inner surface of the skull and their global asymmetries. In: Medical imaging 2011: image process, Vol. 7962, 79620Y. Bellingham, Washington: SPIE - International Society for Optics and Photonics.
Friedrich, P., Forkel, S.J., Amiez, C., Balsters, J.H., Coulon, O., Fan, L. et al. (2021) Imaging evolution of the primate brain: the next frontier? NeuroImage, 228, 117685. Available from: https://doi.org/10.1016/j.neuroimage.2020.117685
Grimaud-Hervé, D. (1997) L'évolution de l'encéphale chez Homo erectus et Homo sapiens: exemples de l'Asie et de l'Europe. Paris: CNRS éditions.
Guevara, P., Poupon, C., Rivière, D., Cointepas, Y., Descoteaux, M., Thirion, B. et al. (2011) Robust clustering of massive tractography datasets. NeuroImage, 54, 1975-1993. Available from: https://doi.org/10.1016/j.neuroimage.2010.10.028
Gunz, P., Neubauer, S., Falk, D., Tafforeau, P., le Cabec, A., Smith, T.M. et al. (2020) Australopithecus afarensis endocasts suggest ape-like brain organization and prolonged brain growth. Science Advances, 6(14), eaaz4729gunz. Available from: https://doi.org/10.1126/sciadv.aaz4729
Holloway, R.L., Broadfield, D.C. & Yuan, M.S. (2004) Brain endocasts the paleoneurological evidence, Vol. 3. Hoboken, NJ: John Wiley and Sons, Inc.
Hopkins, W.D., Sprung-Much, T., Amiez, C., Procyk, E., Petrides, M., Schapiro, S.J. et al. (2022) A comprehensive analysis of variability in the sulci that define the inferior frontal gyrus in the chimpanzee (Pan troglodytes) brain. American Journal of Biological Anthropology, 179, 31-47.
Jerison, H.J. (1973) Evolution of the brain and intelligence. New York: Academic Press.
Juch, H., Zimine, I., Seghier, M.L., Lazeyras, F. & Fase, J.H.D. (2005) Anatomical variability of the lateral frontal lobe surface: implication for intersubject variability in language neuroimaging. NeuroImage, 24, 504-514. Available from: https://doi.org/10.1016/j.neuroimage.2004.08.037
Kochiyama, T., Ogihara, N., Tanabe, H.C., Kondo, O., Amano, H., Hasegawa, K. et al. (2018) Reconstructing the Neanderthal brain using computational anatomy. Scientific Reports, 8, 6296.
Le Gros Clark, W.E., Cooper, D.M. & Zuckerman, S. (1936) The endocranial cast of the chimpanzee. Journal of the Royal Anthropological Institute, 66, 249-268.
Maddah, M., Grimson, W.E.L., Warfield, S.K. & Wells, W.M. (2008) A unified framework for clustering and quantitative analysis of white matter fiber tracts. Medical Image Analysis, 12, 191-202. Available from: https://doi.org/10.1016/j.media.2007.10.003
Mai, S.T., Goebl, S. & Plant, C. (2012) A similarity model and segmentation algorithm for White matter fiber tracts. In: 2012 IEEE 12th International Conference on Data Mining. Presented at the 2012 IEEE 12th International Conference on Data Mining (ICDM). Brussels, Belgium: IEEE, pp. 1014-1019. Available from: https://doi.org/10.1109/ICDM.2012.95
Mangin, J.-F., Le Guen, Y., Labra, N., Grigis, A., Frouin, V., Guevara, M. et al. (2019) “Plis de passage” deserve a role in models of the cortical folding process. Brain Topography, 32, 1035-1048. Available from: https://doi.org/10.1007/s10548-019-00734-8
Mangin, J.-F., Riviere, D., Cachia, A., Duchesnay, E., Cointepas, Y., Papadopoulos-Orfanos, D. et al. (2004) Object-based morphometry of the cerebral cortex. IEEE Transactions on Medical Imaging, 23, 968-982. Available from: https://doi.org/10.1109/TMI.2004.831204
Mellerio, C., Lapointe, M.N., Roca, P., Charron, S., Legrand, L., Meder, J.F. et al. (2016) Identification of reliable Sulcal patterns of the human Rolandic region. Frontiers in Human Neuroscience, 17, 10-410.
Miller, J.A. & Weiner, K.S. (2022) Unfolding the evolution of human cognition. Trends in Cognitive Sciences, 26(9), 735-737.
Neubauer, S., Hublin, J.J. & Gunz, P. (2018) The evolution of modern human brain shape. Science Advances, 4(1), eaao5961. Available from: https://doi.org/10.1126/sciadv.aao5961
Nowinski, W.L. (2022) On the definition, construction, and presentation of the human cerebral sulci: a morphology-based approach. Journal of Anatomy, 241(3), 789-808.
Ono, M., Kubik, S. & Abernathey, C.A. (1990) Atlas of cerebral sulci. Verlag, Stuttgart: Thieme-Stratton Corp.
Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O. et al. (2012) Scikit-learn: machine learning in Python. https://doi.org/10.48550/ARXIV.1201.0490
Perrot, M., Rivière, D. & Mangin, J.-F. (2011) Cortical sulci recognition and spatial normalization. Medical Image Analysis, 15, 529-550. Available from: https://doi.org/10.1016/j.media.2011.02.008
Ponce de León, M.S., Bienvenu, T., Marom, A., Engel, S., Tafforeau, P., Alatorre Warren, J.L. et al. (2021) The primitive brain of early Homo. Science, 372(6538), 165-171. Available from: https://doi.org/10.1126/science.aaz0032
Robson, M.D., Gatehouse, P.D., Bydder, M. & Bydder, G.M. (2003) Magnetic resonance: an introduction to ultrashort TE (UTE) imaging. Journal of Computer Assisted Tomography, 27, 825-846. Available from: https://doi.org/10.1097/00004728-200311000-00001
Sørensen, T. (1948) A method of establishing groups of equal amplitude in plant sociology based on similarity of species content and ist application to analyses of the vegetation on Danish commons. Copenhagen: Det Kongelige Danske Videnskabernes Selskab. Munksgaard.
Zollikofer, P.E., Bienvenu, T., Suwa, G., Asfaw, B., White, T.D. & Ponce de León, M.S. (2022) Endocranial ontogeny and evolution on early Homo sapiens: the evidence from Herto, Ethiopia. Proceedings of the National Academy of Sciences, 119(32), e2123553119.