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Networking Brains: Modeling Spatial Relationships of the Cerebral Cortex

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Digital Endocasts

Abstract

Brain mapping has always been a priority in neurobiology and evolutionary neuroanatomy. In the last century, methodological issues and technical advances have generated a vivid debate on the parcellation and functions of the cortical territories. Brain structure is generally analyzed by considering the network of connections associated with neural pathways. Nonetheless, there is still a major debate on the recognition of the spatial and geometrical components of the cerebral cortex. The maps produced by Korbinian Brodmann in the early twentieth century on the basis of histological patterns represented a pioneering and decisive step in this sense, being a reference until the present day. Network models allow a numerical analysis of the spatial relationships among anatomical elements, supplying a quantitative tool to evaluate their reciprocal geometrical organization. This approach is able to analyze the spatial parameters associated with an anatomical system, characterized by the relationships of its elements. The network analysis of the spatial contiguity of Brodmann’s areas approximately describes the major cerebral lobes. A frontal cluster includes only the prefrontal areas. There is a large parieto-occipital block including also the precentral and paracentral cortex. The cortical areas identified by the model match different areas of craniocerebral relationships, namely, the anterior fossa influenced by the upper face (prefrontal cortex), the middle fossa influenced by cranial base and mandibular integration (temporal cortex), and the vault which is characterized by more linear brain-bone dynamics (parieto-occipital cortex). The maps of Brodmann, after one century of contributions, are now replaced by finer parcellations obtained with new technical approaches based on histology, biochemistry, and metabolism, enhanced by advances in brain imaging and digital biology. Besides issues associated with cognitive processing, structural factors can influence geometrical and mechanical properties of the cerebral morphology. Network theory, applied to alternative parcellation schemes or to specific brain districts, can provide essential information on evolutionary factors channeling or constraining the evolution of the brain spatial organization.

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References

  • Ackerley R, Kavounoudias A (2015) The role of tactil afference in shaping motor behaviour and implications for prosthetic innovation. Neuropsychologia 79:192–205

    Article  Google Scholar 

  • Alexander-Bloch A, Giedd JN, Bullmore E (2013) Imaging structural co-variance between human brain regions. Nat Rev Neurosci 14:322–336

    Article  Google Scholar 

  • Allen JS, Damasio H, Grabowski TJ (2002) Normal neuroanatomical variation in the human brain: an MRI-volumetric study. Am J Phys Anthropol 118:341–358

    Article  Google Scholar 

  • Amunts K, Zilles K (2012) Architecture and organizational principles of Broca’s region. Trends Cogn Sci 16:418–426

    Article  Google Scholar 

  • Amunts K, Schleicher A, Burgel U, Mohlberg H, Uylings HBM, Zilles K (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412:319–341

    Article  Google Scholar 

  • Annese J (2009) In retrospect: Brodmann’s brain map. Nature 461:884

    Article  Google Scholar 

  • Bastir M, Rosas A (2005) Hierarchical nature of morphological integration and modularity in the human posterior face. Am J Phys Anthropol 128:26–34

    Article  Google Scholar 

  • Bastir M, Rosas A (2006) Correlated variation between the lateral basicranium and the face: a geometric morphometric study in different human groups. Arc Oral Biol 51:814–824

    Article  Google Scholar 

  • Bastir M, Rosas A, Kuroe K (2004) Petrosal orientation and mandibular ramus breadth: evidence for an integrated petroso-mandibular developmental unit. Am J Phys Anthropol 123:340–350

    Article  Google Scholar 

  • Bastir M, Rosas A, Lieberman DE, O’Higgins P (2008) Middle craneal fossa and the origin of modern humans. Anat Rec 291:130–140

    Article  Google Scholar 

  • Bayly PV, Taber LA, Kroenke CD (2014) Mechanical forces in cerebral cortical folding: a review of measurements and models. J Mech Behav Biomed Mater 29:568–581

    Article  Google Scholar 

  • Bruner E (2004) Geometric morphometrics and paleoneurology: brain shape evolution in the genus homo. J Hum Evol 47:279–303

    Article  Google Scholar 

  • Bruner E (2015) Functional craniology and brain evolution. In: Bruner E (ed) Human paleoneurology. Springer, Cham, pp 57–94

    Google Scholar 

  • Bruner E, Holloway R (2010) Bivariate approach to the widening of the frontal lobes in the genus homo. J Hum Evol 58:138–146

    Article  Google Scholar 

  • Bruner E, Iriki A (2016) Extending mind, visuospatial integration, and the evolution of the parietal lobes in the human genus. Quat Int 405:98–110

    Article  Google Scholar 

  • Bruner E, Ripani M (2008) A quantitative and descriptive approach to morphological variation of the endocranial base in modern humans. Am J Phys Anthropol 137:30–40

    Article  Google Scholar 

  • Bruner E, Manzi G, Arsuaga JL (2003) Encephalization and allometric trajectories in the genus Homo: evidence from the Neanderthal and modern lineages. Proc Natl Acad Sci U S A 100:15335–15340

    Article  Google Scholar 

  • Bruner E, Martin-Loeches M, Colom R (2010) Human midsagittal brain shape variation: patterns, allometry and integration. J Anat 216:589–599

    Article  Google Scholar 

  • Bruner E, Mantini S, Musso F, de la Cuétara JM, Ripani M, Sherkat S (2011) The evolution of the meningeal vascular system in the human genus: from brain shape to thermoregulation. Am J Hum Biol 23:35–43

    Article  Google Scholar 

  • Bruner E, De la Cuétara M, Musso F (2012) Quantifying patterns of endocranial heat distribution: brain geometry and thermoregulation. Am J Hum Biol 24:753–762

    Article  Google Scholar 

  • Bruner E, de la Cuétara JM, Masters M, Amano H, Ogihara N (2014) Functional craniology and brain evolution: from paleontology to biomedicine. Front Neuroanat 8:19

    Article  Google Scholar 

  • Bruner E, Amano H, de la Cuétara JM, Ogihara N (2015) The brain and the braincase: a spatial analysis on the midsagittal profile in adult humans. J Anat 227:268–276

    Article  Google Scholar 

  • Bruner E, Preuss T, Chen X, Rilling J (2017) Evidence for expansion of the precuneus in human evolution. Brain Struct Funct 222:1053–1060

    Article  Google Scholar 

  • Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13:336–349

    Google Scholar 

  • Caminiti R, Innocenti GM, Battaglia-Mayer A (2015) Organization and evolution of parieto-frontal processing streams in macaque monkeys and humans. Neuosci Biobehav Rev 56:73–96

    Article  Google Scholar 

  • Chen CH, Gutierrez ED, Thompson W, Panizzon MS, Jernigan TL, Eyler LT, Fennema-Notestine C, Jak AJ, Neale MC, Franz CE, Lyons MJ, Grant MD, Fischl B, Seidman LJ, Tsuang MT, Kremen WS, Dale AM (2012) Hierarchical genetic organization of human cortical surface area. Science 335:1634–1636

    Article  Google Scholar 

  • Clark A (2007) Re-inventing ourselves: the plasticity of embodiment, sensing, and mind. J Med Philos 32:263–282

    Article  Google Scholar 

  • Clark A (2008) Supersizing the mind. Embodiment, action, and cognitive extension. Oxford University Press, Oxford

    Book  Google Scholar 

  • Craddock RC, Jbabdi S, Yan CG, Vogelstein JT, Castellanos FX, Di Martino A, Kelly C, Heberlein K, Colcombe S, Milham MP (2013) Imaging human connectomes at the macroscale. Nat Methods 10:524–539

    Article  Google Scholar 

  • Crispo E (2007) The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61:2469–2479

    Article  Google Scholar 

  • De Sousa AA, Sherwood CC, Mohlberg H, Amunts K, Schleicher A, MacLeod CE, Hof PR, Frahm H, Zilles K (2010) Hominoid visual brain structure volumes and the position of the lunate sulcus. J Hum Evol 58:281–292

    Article  Google Scholar 

  • Eickhoff S, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25:1325–1335

    Article  Google Scholar 

  • Eidelberg D, Galaburda AM (1984) Inferior parietal lobule. Arch Neurol 41:843–852

    Article  Google Scholar 

  • Esteve-Altava B (2015) An R implementation of an algorithm to detect hierarchical, overlapping modules in networks. Applications to the human skull. Figshare, https://dx.doi.org/10.6084/m9.figshare.1577668.v1

  • Esteve-Altava B, Marugán-Lobón J, Bastir M, Botella H, Rasskin-Gutman D (2013) Grist for Riedl’s mill: a network model perspective on the integration and modularity of the human skull. J Exp Zool B 320:489–500

    Article  Google Scholar 

  • Fan CC, Bartsch H, Schork AJ, Chen CH, Wang Y, Lo MT, Brown TT, Kuperman JM, Hagler DJ Jr, Schork NJ, Jernigan TL, Dale AM, the Pediatric Imaging, Neurocognition, and Genetics Study (2015) Modeling the 3D geometry of the cortical surface with genetic ancestry. Curr Biol 25:1988–1992

    Article  Google Scholar 

  • Fortunato S (2010) Community detection in graphs. Phys Rep 486:75–174

    Article  Google Scholar 

  • Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, Ugurbil K, Andersson J, Beckmann CF, Jenkinson M, Smith SM, Van Essen DC (2016) A multi-modal parcellation of human cerebral cortex. Nature 536:171–178

    Article  Google Scholar 

  • Goldenberg G (2004) The life of Phineas gage – stories and realities. Cortex 40:552–555

    Article  Google Scholar 

  • Gómez-Robles A, Hopkins WD, Sherwood CC (2014) Modular structure facilitates mosaic evolution of the brain in chimpanzees and humans. Nat Commun 5:4469

    Article  Google Scholar 

  • Gómez-Robles A, Hopkins WD, Schapiro SJ, Sherwood CC (2015) Relaxed genetic control of cortical organization in human brains compared with chimpanzees. Proc Natl Acad Sci U S A 112:14799–804

    Article  Google Scholar 

  • Goriely A, Geers MGD, Holzapfel GA, Jayamohan J, Jérusalem A, Sivaloganathan S, Squier W, Van Dommelen JAW, Waters S, Kuhl E (2015) Mechanics of the brains: perspectives, challenges, and opportunities. Biomech Model Mechanobiol 14:931–965

    Article  Google Scholar 

  • Gould SJ (1977) Ontogeny and phylogeny. Belknap Press, Harvard University Press, Cambridge MA

    Google Scholar 

  • Gunz P, Harvati K (2007) The Neanderthal “chignon”: variation, integration, and homology. J Hum Evol 52:262–274

    Article  Google Scholar 

  • Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159

    Article  Google Scholar 

  • Hilgetag CC, Barbas H (2005) Developmental mechanics of the primate cerebral cortex. Anat Embryol 210:411–417

    Article  Google Scholar 

  • Hilgetag CC, Barbas H (2006) Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol 2:e22

    Article  Google Scholar 

  • Hofman MA (2012) Design principles of the human brain: an evolutionary perspective. Progr Brain Res 195:373–390

    Article  Google Scholar 

  • Humphries MD, Gurney K (2008) Network ‘small-worldness’: a quantitative method for determining canonical network equivalence. PLoS One 3:e0002051

    Article  Google Scholar 

  • Iriki A, Sakura O (2008) The neuroscience of primate intellectual evolution: natural selection and passive and intentional niche construction. Phil Trans R Soc London B 363:2229–2241

    Article  Google Scholar 

  • Iriki A, Taoka M (2012) Triadic (ecological, neural, cognitive) niche construction: a scenario of human brain evolution extrapolating tool use and language from the control of reaching actions. Phil Trans R Soc Lond B 367:10–23

    Article  Google Scholar 

  • Judaš M, Cepanec M, Sedmak G (2012) Brodmann’s map of the human cerebral cortex – or Brodmann’s maps? Translat Neurosci 3:67–74

    Google Scholar 

  • Lieberman DE, Ross CF, Ravosa MJ (2000) The primate cranial base: ontogeny, function, and integration. Y Phys Anthropol 43:117–169

    Article  Google Scholar 

  • Malafouris L (2010) The brain-artefact Interface (BAI): a challenge for archaeology and cultural neuroscience. Soc Cogn Affect Neurosci 5:264–273

    Article  Google Scholar 

  • Malafouris L (2013) How things shape the mind: a theory of material engagement. MIT Press, Cambridge

    Google Scholar 

  • Meunier D, Lambiotte R, Bullmore ET (2010) Modular and hierarchically modular organization of brain networks. Front Neurosci 4:200

    Article  Google Scholar 

  • Mitteroecker P, Bookstein F (2008) The evolutionary role of modularity and integration in the hominoid cranium. Evolution 62:943–958

    Article  Google Scholar 

  • Mitteroecker P, Gunz P (2009) Advances in geometric morphometrics. Evol Biol 36:235–247

    Article  Google Scholar 

  • Pearce JMS (2005) Brodmann’s cortical maps. J Neurol Neurosurg Psychiatry 76:259

    Article  Google Scholar 

  • Preuss TM (2011) The human brain: rewired and running hot. Ann N Y Acad Sci 1225(S1):E182–E191

    Article  Google Scholar 

  • Quallo MM, Price CJ, Ueno K, Asamizuya T, Cheng K, Lemon RN, Iriki A (2009) Gray and white matter changes associated with tool-use learning in macaque monkeys. Proc Natl Acad Sci U S A 106:18379–18384

    Article  Google Scholar 

  • Raichle ME (2003) Functional brain imaging and human brain function. J Neurosci 23:3959–3962

    Google Scholar 

  • Raichle ME (2010) Two views of brain functions. Trends Cogn Sci 14:180–190

    Article  Google Scholar 

  • Rakic P (2004) Genetic control of cortical convolutions. Science 303:1983–1984

    Article  Google Scholar 

  • Rasskin-Gutman D, Buscalioni AD (2001) Theoretical morphology of the Archosaur (Reptilia: Diapsida) pelvic girdle. Paleobiology 27:59–78

    Article  Google Scholar 

  • Rasskin-Gutman D, Esteve-Altava B (2014) Connecting the dots: anatomical network analysis in morphological EvoDevo. Biol Theor 9:178–193

    Article  Google Scholar 

  • Ribas GC, Yasuda A, Ribas EC, Nishikuni K, Rodrigues AJ (2006) Surgical anatomy of microneurosurgical sulcal key-points. Neurosurgery 59:S177–S208

    Google Scholar 

  • Richtsmeier JT, Aldridge K, de Leon VB, Panchal J, Kane AA, Marsh JL, Yan P, Cole TM (2006) Phenotypic integration of neurocranium and brain. J Exp Zool 306B:360–378

    Article  Google Scholar 

  • Rilling JK (2006) Human and non-human primate brains: are they allometrically scaled versions of the same design? Evol Anthropol 15:65–67

    Article  Google Scholar 

  • Rilling JK (2008) Neuroscientific approaches and applications within anthropology. Yrb Phys Anthropol 51:2–32

    Article  Google Scholar 

  • Rilling JK (2014) Comparative primate neuroimaging: insights into human brain evolution. Trends Cogn Sci 18:45–55

    Article  Google Scholar 

  • Rilling JK, Seligman RA (2002) A quantitative morphometric comparative analysis of the primate temporal lobe. J Hum Evol 42:505–533

    Article  Google Scholar 

  • Semendeferi K, Damasio H (2000) The brain and its main anatomical subdivisions in living hominoids using magneticresonance imaging. J Hum Evol 38:317–332

    Article  Google Scholar 

  • Shen H, Cheng X, Cai K, Hu MB (2009) Detect overlapping and hierarchical community structure in networks. Phys A Stat Mech Appl 388:1706–1712

    Article  Google Scholar 

  • Sherwood CC, Smaers JB (2013) What’s the fuss over human frontal lobe evolution? Trends Cogn Sci 17:432–433

    Article  Google Scholar 

  • Šimić G, Hof PR (2015) In search of the definitive Brodmann’s map of cortical areas in humans. J Comp Neurol 523:5–14

    Article  Google Scholar 

  • Sporns O, Chialvo DR, Kaiser M, Hilgetag CC (2004) Organization, development and functions of complex brain networks. Trend Cogn Sci 8:418–425

    Article  Google Scholar 

  • Tallinen T, Chung JY, Rousseau F, Girard N, Lefèvre J, Mahadevan L (2016) On the growth and form of cortical convolutions. Nat Phys 12:588–593

    Article  Google Scholar 

  • Thompson D’AW (1942) On growth and form. Cambridge University Press, Cambridge

    Google Scholar 

  • Toga AW, Thompson PM, Mori S, Amunts K, Zilles K (2006) Towards multimodal atlases of the human brain. Nat Rev Neurosci 7:952–966

    Article  Google Scholar 

  • Toro R (2012) On the possible shapes of the brain. Evol Biol 39:600–612

    Article  Google Scholar 

  • Toro R, Burnod Y (2005) A morphogenetic model for the development of cortical convolutions. Cereb Cortex 15:1900–1913

    Article  Google Scholar 

  • Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318

    Article  Google Scholar 

  • Van Essen DC, Dierker DL (2007) Surface-based and probabilistic atlases of primate cerebral cortex. Neuron 56:209–225

    Article  Google Scholar 

  • Zilles K, Amunts K (2010) Centenary of Brodmann’s map – conception and fate. Nat Rev Neurosci 11:139–145

    Article  Google Scholar 

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Acknowledgments

EB is funded by the Spanish Government (CGL2015-65387-C3-3-P). BEA is funded by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No. 654155. DRG is funded by Spanish MINECO/FEDER (BFU2015-70927-R).

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Bruner, E., Esteve-Altava, B., Rasskin-Gutman, D. (2018). Networking Brains: Modeling Spatial Relationships of the Cerebral Cortex. 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_13

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