A network approach to brain form, cortical topology and human evolution

Network analysis provides a quantitative tool to investigate the topological properties of a system. In anatomy, it can be employed to investigate the spatial organization of body parts according to their contiguity and patterns of physical contact. In this study, we build a model representing the spatial adjacency of the major regions of the human brain often considered in evolutionary neuroanatomy, to analyse its topological features. Results suggest that the frontal lobe is topologically independent of the posterior regions of the brain, which in turn are more integrated and influenced by reciprocal constraints. The precentral gyrus represents a hinge between the anterior and posterior blocks. The lateral temporal cortex is particularly influenced by the neighbouring regions, while the parietal cortex is minimally constrained by the overall brain organization. Beyond the reciprocal spatial influences among cortical areas, brain form is further constrained by spatial and mechanical influence of the braincase, including bone and connective elements. The anterior fossa and the parietal bones are the elements more sensitive to the brain–braincase spatial organization. These topological properties must be properly considered when making inferences on evolutionary variations and macroscopic differences of the human brain morphology.

[1]  P. Bonacich Power and Centrality: A Family of Measures , 1987, American Journal of Sociology.

[2]  Phillip Bonacich,et al.  Eigenvector-like measures of centrality for asymmetric relations , 2001, Soc. Networks.

[3]  E. Bruner The Brain, the Braincase, and the Morphospace , 2018 .

[4]  D. V. van Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system. , 1997, Nature.

[5]  R. Holloway,,et al.  Brain endocasts - the paleoneurological evidence , 2004 .

[6]  A. Rosas,et al.  Hierarchical nature of morphological integration and modularity in the human posterior face. , 2005, American journal of physical anthropology.

[7]  M. de la Rasilla,et al.  Temporal Lobe Sulcal Pattern and the Bony Impressions in the Middle Cranial Fossa: The Case of the El Sidrón (Spain) Neandertal Sample , 2014, Anatomical record.

[8]  A. Dale,et al.  Hierarchical Genetic Organization of Human Cortical Surface Area , 2012, Science.

[9]  D. V. Essen,et al.  Surface-Based and Probabilistic Atlases of Primate Cerebral Cortex , 2007, Neuron.

[10]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[11]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[12]  E. Bruner Language, Paleoneurology, and the Fronto-Parietal System , 2017, Front. Hum. Neurosci..

[13]  Giorgio M. Innocenti,et al.  Organization and evolution of parieto-frontal processing streams in macaque monkeys and humans , 2015, Neuroscience & Biobehavioral Reviews.

[14]  R. McCarthy,et al.  Anthropoid cranial base architecture and scaling relationships. , 2001, Journal of human evolution.

[15]  Naomichi Ogihara,et al.  Functional craniology and brain evolution: from paleontology to biomedicine , 2014, Front. Neuroanat..

[16]  R. Sotero,et al.  From Blood Oxygenation Level Dependent (BOLD) Signals to Brain Temperature Maps , 2010, Bulletin of mathematical biology.

[17]  Robert D. Acland,et al.  Color atlas of anatomy. A photographic study of the human body , 1987 .

[18]  Andrea Landherr,et al.  A Critical Review of Centrality Measures in Social Networks , 2010, Bus. Inf. Syst. Eng..

[19]  J. Lefévre,et al.  On the growth and form of cortical convolutions , 2016, Nature Physics.

[20]  D. Lieberman,et al.  The primate cranial base: ontogeny, function, and integration. , 2000, American journal of physical anthropology.

[21]  P V Bayly,et al.  Mechanical forces in cerebral cortical folding: a review of measurements and models. , 2014, Journal of the mechanical behavior of biomedical materials.

[22]  James K Rilling,et al.  Precuneus proportions and cortical folding: A morphometric evaluation on a racially diverse human sample. , 2017, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[23]  E. Kuhl,et al.  Mechanics of the brain: perspectives, challenges, and opportunities , 2015, Biomechanics and Modeling in Mechanobiology.

[24]  E. Bruner Human paleoneurology: Shaping cortical evolution in fossil hominids , 2019, The Journal of comparative neurology.

[25]  Leonardo Cerliani,et al.  Structural Variability Across the Primate Brain: A Cross-Species Comparison , 2018, Cerebral cortex.

[26]  Mathieu Bastian,et al.  Gephi: An Open Source Software for Exploring and Manipulating Networks , 2009, ICWSM.

[27]  L. Radinsky The fossil evidence of anthropoid brain evolution , 2005 .

[28]  Matthew F. Glasser,et al.  Development and Evolution of Cerebral and Cerebellar Cortex , 2018, Brain, Behavior and Evolution.

[29]  B. Esteve-Altava,et al.  Concept of Burden in Evo-Devo , 2021, Evolutionary Developmental Biology.

[30]  Challenges in Identifying and Interpreting Organizational Modules in Morphology , 2017 .

[31]  D. Lieberman,et al.  Middle cranial fossa anatomy and the origin of modern humans. , 2008, Anatomical record.

[32]  V. Abdala,et al.  Network architecture associated with the highly specialized hindlimb of frogs , 2017, PloS one.

[33]  D. Rasskin-Gutman,et al.  Connecting the Dots: Anatomical Network Analysis in Morphological EvoDevo , 2014 .

[34]  P. Gunz,et al.  The Neanderthal "chignon": variation, integration, and homology. , 2007, Journal of human evolution.

[35]  Roberto Toro,et al.  On the Possible Shapes of the Brain , 2012, Evolutionary Biology.

[36]  Kristina Lerman,et al.  Rethinking Centrality: The Role of Dynamical Processes in Social Network Analysis , 2012, ArXiv.

[37]  Emiliano Bruner,et al.  A bivariate approach to the widening of the frontal lobes in the genus Homo. , 2010, Journal of human evolution.

[38]  E. Bruner Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo. , 2004, Journal of human evolution.

[39]  Lianne H. Scholtens,et al.  Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees , 2019, Proceedings of the National Academy of Sciences.

[40]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[41]  E. Bruner 4.05 – The Fossil Evidence of Human Brain Evolution , 2017 .

[42]  N. Ogihara,et al.  The brain and the braincase: a spatial analysis on the midsagittal profile in adult humans , 2015, Journal of anatomy.

[43]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[44]  L. Altenberg,et al.  PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY , 1996, Evolution; international journal of organic evolution.

[45]  J. Richtsmeier,et al.  Phenotypic integration of neurocranium and brain. , 2006, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[46]  C. Sherwood,et al.  Relaxed genetic control of cortical organization in human brains compared with chimpanzees , 2015, Proceedings of the National Academy of Sciences.

[47]  Danielle S Bassett,et al.  Structure, function, and control of the human musculoskeletal network , 2018, PLoS biology.

[48]  B. Esteve-Altava In search of morphological modules: a systematic review , 2017, Biological reviews of the Cambridge Philosophical Society.

[49]  Ana Sofia Pereira-Pedro,et al.  Shape analysis of spatial relationships between orbito‐ocular and endocranial structures in modern humans and fossil hominids , 2017, Journal of anatomy.

[50]  Claus C. Hilgetag,et al.  Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex , 2006, PLoS Comput. Biol..

[51]  Kristina Lerman,et al.  A Parameterized Centrality Metric for Network Analysis , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  Lorena R. R. Gianotti,et al.  Functional brain network efficiency predicts intelligence , 2012, Human brain mapping.

[53]  Leonard M. Freeman,et al.  A set of measures of centrality based upon betweenness , 1977 .

[54]  John S. Allen,et al.  Normal neuroanatomical variation in the human brain: an MRI-volumetric study. , 2002, American journal of physical anthropology.

[55]  K. Nishikuni,et al.  Surgical Anatomy of Microneurosurgical Sulcal Key Points , 2006, Neurosurgery.

[56]  Y. Burnod,et al.  A morphogenetic model for the development of cortical convolutions. , 2005, Cerebral cortex.

[57]  D. Rasskin-Gutman,et al.  Beyond the functional matrix hypothesis: a network null model of human skull growth for the formation of bone articulations , 2014, Journal of anatomy.

[58]  B. Franke,et al.  Neandertal Introgression Sheds Light on Modern Human Endocranial Globularity , 2018, Current Biology.

[59]  M E J Newman,et al.  Finding and evaluating community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[60]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[61]  D. Rasskin-Gutman,et al.  Grist for Riedl's mill: a network model perspective on the integration and modularity of the human skull. , 2013, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[62]  C. T. Butts,et al.  Revisiting the Foundations of Network Analysis , 2009, Science.

[63]  A. Rosas,et al.  Petrosal orientation and mandibular ramus breadth: evidence for an integrated petroso-mandibular developmental unit. , 2004, American journal of physical anthropology.

[64]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[65]  Günter P. Wagner,et al.  Complex Adaptations and the Evolution of Evolvability , 2005 .

[66]  Julia M. Huntenburg,et al.  Large-Scale Gradients in Human Cortical Organization , 2018, Trends in Cognitive Sciences.

[67]  A. Schleicher,et al.  The human pattern of gyrification in the cerebral cortex , 2004, Anatomy and Embryology.

[68]  E. Bruner Human Paleoneurology and the Evolution of the Parietal Cortex , 2018, Brain, Behavior and Evolution.

[69]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[70]  M L Moss,et al.  A functional approach to craniology. , 1960, American journal of physical anthropology.

[71]  H. Barbas,et al.  Developmental mechanics of the primate cerebral cortex , 2005, Anatomy and Embryology.

[72]  R. Kahn,et al.  Aberrant Frontal and Temporal Complex Network Structure in Schizophrenia: A Graph Theoretical Analysis , 2010, The Journal of Neuroscience.

[73]  Borja Esteve-Altava,et al.  Anatomical Network Analysis in Evo-Devo , 2021, Evolutionary Developmental Biology.

[74]  HERBERT A. SIMON,et al.  The Architecture of Complexity , 1991 .

[75]  H. Damasio,et al.  The brain and its main anatomical subdivisions in living hominoids using magnetic resonance imaging. , 2000, Journal of human evolution.

[76]  Gábor Csárdi,et al.  The igraph software package for complex network research , 2006 .

[77]  Ana Sofia Pereira-Pedro,et al.  Patterns of morphological integration between parietal and temporal areas in the human skull , 2017, Journal of morphology.

[78]  Ralph L. Holloway,et al.  The Human Fossil Record , 2004 .

[79]  Joan T. Richtsmeier,et al.  Hand in glove: brain and skull in development and dysmorphogenesis , 2013, Acta Neuropathologica.

[80]  T. F. Hansen,et al.  Predicting evolutionary potential: A numerical test of evolvability measures , 2019, Evolution; international journal of organic evolution.

[81]  Patrick C Phillips,et al.  Network thinking in ecology and evolution. , 2005, Trends in ecology & evolution.

[82]  C. Sherwood,et al.  Brain Plasticity and Human Evolution , 2017 .

[83]  A. Rosas,et al.  Craniofacial levels and the morphological maturation of the human skull , 2006, Journal of anatomy.

[84]  A. Gómez‐Robles,et al.  Exceptional Evolutionary Expansion of Prefrontal Cortex in Great Apes and Humans , 2017, Current Biology.

[85]  Andreas Daffertshofer,et al.  Network structure of the human musculoskeletal system shapes neural interactions on multiple time scales , 2018, Science Advances.

[86]  A. Schleicher,et al.  Gyrification in the cerebral cortex of primates. , 1989, Brain, behavior and evolution.

[87]  O. Sporns,et al.  The economy of brain network organization , 2012, Nature Reviews Neuroscience.

[88]  Terri Gullickson Human Brain Anatomy in Computerized Images. , 1995 .

[89]  E. Bruner,et al.  Networking Brains: Modeling Spatial Relationships of the Cerebral Cortex , 2018 .

[90]  Michel A Hofman,et al.  Design principles of the human brain: an evolutionary perspective. , 2012, Progress in brain research.

[91]  E. Bruner Functional Craniology, Human Evolution, and Anatomical Constraints in the Neanderthal Braincase , 2014 .

[92]  Santo Fortunato,et al.  Finding Statistically Significant Communities in Networks , 2010, PloS one.

[93]  B. Esteve-Altava,et al.  Network models in anatomical systems. , 2011, Journal of anthropological sciences = Rivista di antropologia : JASS.

[94]  Robin I. M. Dunbar,et al.  New insights into differences in brain organization between Neanderthals and anatomically modern humans , 2013, Proceedings of the Royal Society B: Biological Sciences.

[95]  Giorgio Manzi,et al.  Evolution of the base of the brain in highly encephalized human species. , 2011, Nature communications.

[96]  Mark E. J. Newman A measure of betweenness centrality based on random walks , 2005, Soc. Networks.

[97]  John W Pinney,et al.  Making the right connections: biological networks in the light of evolution , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[98]  E. Bruner Functional Craniology and Brain Evolution , 2015 .

[99]  C. Kroenke,et al.  Mechanics of cortical folding: stress, growth and stability , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[100]  Edward T. Bullmore,et al.  Modular and Hierarchically Modular Organization of Brain Networks , 2010, Front. Neurosci..

[101]  T. White,et al.  Comprar Human Osteology, Third Edition | Pieter Arend Folkens | 9780123741349 | Academic Press , 2010 .

[102]  Edward T. Bullmore,et al.  Neuroinformatics Original Research Article , 2022 .