Abstract
The set of neural connections in an organism is now called the connectome. Using recent noninvasive techniques such as diffusion tensor imaging and traditional invasive techniques for tract tracing has uncovered a wide range of connectomes from Caenorhabditis elegans and Drosophila melanogaster to cat, mouse, rat, macaque, and human. We can therefore start to look at organisational changes during evolution. At the same time cell lineage information and measurements at different time steps allow us to observe network changes during individual, ontogenetic development. We find that the structure of a network is closely linked to its function, with distinct functional components first leading to network modules and, after the rise of further specialisation, to a hierarchical architecture with modules at different levels of network organisation. We first describe concepts that are used to characterize complex networks, then move on to briefly discuss computational models for development and evolution, before showing how network features change during the evolution and development of brain networks. We conclude with future challenges in the field of connectome development and evolution.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Achacoso TB, Yamamoto WS (1992) AY’s neuroanatomy of C. elegans for computation. CRC Press, Boca Raton
Amaral LAN, Scala A, Barthélémy M, Stanley HE (2000) Classes of small-world networks. Proc Natl Acad Sci USA 97(21):11149–11152
Ball G, Aljabar P, Zebari S, Tusor N, Arichi T, Merchant N, Robinson EC, Ogundipe E, Rueckert D, Edwards AD, Counsell SJ (2014) Rich-club organization of the newborn human brain. Proc Natl Acad Sci USA 111(20):7456–7461. doi:10.1073/pnas.1324118111
Barabási A-L, Albert R (1999) Emergence of scaling in random networks. Science 286:509–512
Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A (2008) Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci 28(37):9239–9248
Bauer R, Zubler F, Hauri A, Muir DR, Douglas RJ (2012) Developmental origin of patchy axonal connectivity in the neocortex: a computational model. Cereb Cortex. doi:10.1093/cercor/bhs327
Bauer R, Zubler F, Pfister S, Hauri A, Pfeiffer M, Muir DR, Douglas RJ (2014) Developmental self-construction and -configuration of functional neocortical neuronal networks. PLoS Comput Biol 10(12):e1003994. doi:10.1371/journal.pcbi.1003994
Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13(5):336–349
Buzas P, Kovacs K, Ferecsko AS, Budd JM, Eysel UT, Kisvarday ZF (2006) Model-based analysis of excitatory lateral connections in the visual cortex. J Comp Neurol 499(6):861–881. doi:10.1002/cne.21134
Cardona A, Saalfeld S, Preibisch S, Schmid B, Cheng A, Pulokas J, Tomancak P, Hartenstein V (2010) An integrated micro- and macroarchitectural analysis of the Drosophila brain by computer-assisted serial section electron microscopy. PLoS Biol 8(10):e1000502
Chatterjee N, Sinha S (2008) Understanding the mind of a worm: hierarchical network structure underlying nervous system function in C. elegans. Prog Brain Res 168:145–153. doi:10.1016/S0079-6123(07)68012-1
Collin G, van den Heuvel MP (2013) The ontogeny of the human connectome: development and dynamic changes of brain connectivity across the life span. Neuroscientist. doi:10.1177/1073858413503712
Collin G, Sporns O, Mandl RC, van den Heuvel MP (2013) Structural and functional aspects relating to cost and benefit of rich club organization in the human cerebral cortex. Cereb Cortex. doi:10.1093/cercor/bht064
Costa LF, Rodrigues FA, Travieso G, Villas Boas PR (2007) Characterization of complex networks: a survey of measurements. Adv Phys 56(1):167–242
Crossley NA, Mechelli A, Scott J, Carletti F, Fox PT, McGuire P, Bullmore ET (2014) The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain Journal Neurol 137(8):2382–2395. doi:10.1093/brain/awu132
da Costa Fontoura L, Kaiser M, Hilgetag CC (2007) Predicting the connectivity of primate cortical networks from topological and spatial node properties. BMC Syst Biol 1:16
Daianu M, Dennis EL, Jahanshad N, Nir TM, Toga AW, Jack CR, Weiner MW, Thompson PM, Initia ADN (2013) Alzheimer’s disease disrupts rich club organization in brain connectivity networks. I S Biomed Imaging 2013:266–269
de Reus MA, van den Heuvel MP (2013) Rich club organization and intermodule communication in the cat connectome. J Neurosci 33(32):12929–12939. doi:10.1523/JNEUROSCI.1448-13.2013
Ebbesson SOE (1980) The parcellation theory and its relation to interspecific variability in brain organization, evolutionary and ontogenetic development, and neuronal plasticity. Cell Tissue Res 213:179–212
Ebbesson SOE (1984) Evolution and ontogeny of neural circuits. Behav Brain Sci 7(3):321–331
Felleman DJ, van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47
Gauci J, Stanley KO (2010) Autonomous evolution of topographic regularities in artificial neural networks. Neural Comput 22(7):1860–1898. doi:10.1162/neco.2010.06-09-1042
Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3(5):1116–1133
Goymer P (2008) Network biology: why do we need hubs? Nat Rev Genet 9(9):650
Grayson DS, Ray S, Carpenter S, Iyer S, Dias TG, Stevens C, Nigg JT, Fair DA (2014) Structural and functional rich club organization of the brain in children and adults. PLoS One 9(2):e88297. doi:10.1371/journal.pone.0088297
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(7):e159. doi:10.1371/journal.pbio.0060159
Harriger L, van den Heuvel MP, Sporns O (2012) Rich club organization of macaque cerebral cortex and its role in network communication. PLoS One 7(9):e46497. doi:10.1371/journal.pone.0046497
He Y, Chen ZJ, Evans AC (2007) Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex 17(10):2407–2419. doi:10.1093/cercor/bhl149
Hilgetag CC, Hutt MT (2014) Hierarchical modular brain connectivity is a stretch for criticality. Trends Cogn Sci 18(3):114–115. doi:10.1016/j.tics.2013.10.016
Hilgetag CC, Kaiser M (2004) Clustered organization of cortical connectivity. Neuroinformatics 2(3):353–360
Hilgetag CC, O’Neill MA, Young MP (2000) Hierarchical organization of macaque and cat cortical sensory systems explored with a novel network processor. Philos Trans R Soc Lond Ser B 355:71–89
Hill J, Inder T, Neil J, Dierker D, Harwell J, Van Essen D (2010) Similar patterns of cortical expansion during human development and evolution. Proc Natl Acad Sci USA 107(29):13135–13140. doi:10.1073/pnas.1001229107
Hintze A, Adami C (2008) Evolution of complex modular biological networks. PLoS Comput Biol 4(2):e23. doi:10.1371/journal.pcbi.0040023
Hwang K, Hallquist MN, Luna B (2012) The development of hub architecture in the human functional brain network. Cereb Cortex. doi:10.1093/cercor/bhs227
Ito M, Masuda N, Shinomiya K, Endo K, Ito K (2013) Systematic analysis of neural projections reveals clonal composition of the Drosophila brain. Curr Biol 23(8):644–655. doi:10.1016/j.cub.2013.03.015
Jeong H, Tombor B, Albert R, Oltwal ZN, Barabási A-L (2000) The large-scale organization of metabolic networks. Nature 407:651–654
Jeong H, Mason SP, Barabási A-L, Oltvai ZN (2001) Lethality and centrality in protein networks. Nature 411:41–42
Kaiser M (2011) A tutorial in connectome analysis: topological and spatial features of brain networks. Neuroimage 57(3):892–907
Kaiser M (2015) Neuroanatomy: connectome connects fly and Mammalian brain networks. Curr Biol 25(10):R416–R418
Kaiser M, Hilgetag CC (2004a) Modelling the development of cortical networks. Neurocomputing 58–60:297–302
Kaiser M, Hilgetag CC (2004b) Spatial growth of real-world networks. Phys Rev E Stat Nonlinear Soft Matter Phys 69(3):036103
Kaiser M, Varier S (2011) Evolution and development of brain networks: from Caenorhabditis elegans to Homo sapiens. Netw Comput Neural Syst 22:143–147
Kaiser M, Martin R, Andras P, Young MP (2007) Simulation of robustness against lesions of cortical networks. Eur J Neurosci 25(10):3185–3192. doi:10.1111/j.1460-9568.2007.05574.x
Kaiser M, Hilgetag CC, Kötter R (2010) Hierarchy and dynamics of neural networks. Front Neuroinform 4:112. doi:10.3389/fninf.2010.00112
Karbowski J (2001) Optimal wiring principle and plateaus in the degree of separation for cortical neurons. Phys Rev Lett 86(16):3674–3677. doi:10.1103/PhysRevLett.86.3674
Kim JS, Kaiser M (2014) From Caenorhabditis elegans to the human connectome: a specific modular organization increases metabolic, functional and developmental efficiency. Philos Trans R Soc Lond B Biol Sci 369:1653. doi:10.1098/rstb.2013.0529
Koene RA, Tijms B, van Hees P, Postma F, de Ridder A, Ramakers GJ, van Pelt J, van Ooyen A (2009) NETMORPH: a framework for the stochastic generation of large scale neuronal networks with realistic neuron morphologies. Neuroinformatics 7(3):195–210. doi:10.1007/s12021-009-9052-3
Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87:198701
Lim S, Han CE, Uhlhaas PJ, Kaiser M (2013) Preferential detachment during human brain development: age- and sex-specific structural connectivity in diffusion tensor imaging (DTI). Cereb Cortex Adv Online. doi:10.1093/cercor/bht333
Louf R, Jensen P, Barthelemy M (2013) Emergence of hierarchy in cost-driven growth of spatial networks. Proc Natl Acad Sci USA. doi:10.1073/pnas.1222441110
Masuda N, Aihara K (2004) Global and local synchrony of coupled neurons in small-world networks. Biol Cybern 90(4):302–309. doi:10.1007/s00422-004-0471-9
McAuley JJ, Costa LDF, Caetano TS (2007) Rich-club phenomenon across complex network hierarchies. Appl Phys Lett 91(8). doi:10.1063/1.27723951
Meunier D, Lambiotte R, Bullmore ET (2010) Modular and hierarchically modular organization of brain networks. Front Neurosci 4:200. doi:10.3389/fnins.2010.00200
Milgram S (1967) The small-world problem. Psychol Today 1:60–67
Mitchison G, Crick F (1982) Long axons within the striate cortex: their distribution, orientation, and patterns of connection. Proc Natl Acad Sci USA 79(11):3661–3665
Newman MEJ (2003) The structure and function of complex networks. SIAM Rev 45(2):167–256
Newman ME (2006) Modularity and community structure in networks. Proc Natl Acad Sci USA 103(23):8577–8582. doi:10.1073/pnas.0601602103
Nisbach F, Kaiser M (2007) Developmental time windows for spatial growth generate multiple-cluster small-world networks. Eur Phys J B 58(2):185–191
Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, Hirokawa KE, Bohn P, Joines KM, Peng H, Hawrylycz MJ, Phillips JW, Hohmann JG, Wohnoutka P, Gerfen CR, Koch C, Bernard A, Dang C, Jones AR, Zeng H (2014) A mesoscale connectome of the mouse brain. Nature 508(7495):207–214. doi:10.1038/nature13186
Ravasz E, Barabási A-L (2003) Hierarchical organization in complex networks. Phys Rev E 67:026112
Ray S, Miller M, Karalunas S, Robertson C, Grayson DS, Cary RP, Hawkey E, Painter JG, Kriz D, Fombonne E, Nigg JT, Fair DA (2014) Structural and functional connectivity of the human brain in autism spectrum disorders and attention-deficit/hyperactivity disorder: a rich club-organization study. Hum Brain Mapp 35(12):6032–6048. doi:10.1002/hbm.22603
Rockland KS, Lund JS (1982) Widespread periodic intrinsic connections in the tree shrew visual cortex. Science 215(4539):1532–1534
Rockland KS, Lund JS (1983) Intrinsic laminar lattice connections in primate visual cortex. J Comp Neurol 216(3):303–318. doi:10.1002/cne.902160307
Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069. doi:S1053-8119(09)01074-X [pii] 10.1016/j.neuroimage.2009.10.003
Scannell JW, Blakemore C, Young MP (1995) Analysis of connectivity in the cat cerebral cortex. J Neurosci 15(2):1463–1483
Semendeferi K, Teffer K, Buxhoeveden DP, Park MS, Bludau S, Amunts K, Travis K, Buckwalter J (2011) Spatial organization of neurons in the frontal pole sets humans apart from great apes. Cereb Cortex 21(7):1485–1497. doi:10.1093/cercor/bhq191
Senden M, Deco G, de Reus MA, Goebel R, van den Heuvel MP (2014) Rich club organization supports a diverse set of functional network configurations. NeuroImage 96:174–182. doi:10.1016/j.neuroimage.2014.03.066
Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, Greenstein D, Clasen L, Evans A, Rapoport JL (2008) Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 28(14):3586–3594
Sherwood CC, Subiaul F, Zawidzki TW (2008) A natural history of the human mind: tracing evolutionary changes in brain and cognition. J Anat 212(4):426–454. doi:10.1111/j.1469-7580.2008.00868.x
Sporns O (2013) The human connectome: origins and challenges. Neuroimage. doi:10.1016/j.neuroimage.2013.03.023
Sporns O, Bullmore ET (2014) From connections to function: the mouse brain connectome atlas. Cell 157(4):773–775. doi:10.1016/j.cell.2014.04.023
Sporns O, Zwi JD (2004) The small world of the cerebral cortex. Neuroinformatics 2(2):145–162. doi:10.1385/NI:2:2:145
Sporns O, Chialvo DR, Kaiser M, Hilgetag CC (2004) Organization, development and function of complex brain networks. Trends Cogn Sci 8(9):418–425
Sporns O, Tononi G, Kötter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1(4):e42. doi:10.1371/journal.pcbi.0010042
Stam CJ (2014) Modern network science of neurological disorders. Nat Rev Neurosci 15(10):683–695. doi:10.1038/nrn3801
Stanley KO, Miikkulainen R (2002) Evolving neural networks through augmenting topologies. Evol Comput 10(2):99–127. doi:10.1162/106365602320169811
Torben-Nielsen B, De Schutter E (2014) Context-aware modeling of neuronal morphologies. Front Neuroanat 8:92. doi:10.3389/fnana.2014.00092
Towlson EK, Vertes PE, Ahnert SE, Schafer WR, Bullmore ET (2013) The rich club of the C. elegans neuronal connectome. J Neurosci 33(15):6380–6387. doi:10.1523/JNEUROSCI.3784-12.2013
van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31(44):15775–15786. doi:10.1523/jneurosci.3539-11.2011
van den Heuvel MP, Kahn RS, Goni J, Sporns O (2012) High-cost, high-capacity backbone for global brain communication. Proc Natl Acad Sci USA 109(28):11372–11377. doi:10.1073/pnas.1203593109
van den Heuvel MP, Kersbergen KJ, de Reus MA, Keunen K, Kahn RS, Groenendaal F, de Vries LS, Benders MJ (2014) The neonatal connectome during preterm brain development. Cereb Cortex. doi:10.1093/cercor/bhu095
Van Hooser SD, Heimel JA, Chung S, Nelson SB (2006) Lack of patchy horizontal connectivity in primary visual cortex of a mammal without orientation maps. J Neurosci 26(29):7680–7692. doi:10.1523/JNEUROSCI.0108-06.2006
Varier S, Kaiser M (2011) Neural development features: spatio-temporal development of the Caenorhabditis elegans neuronal network. PLoS Comput Biol 7:e1001044. doi:10.1371/journal.pcbi.1001044
Verbancsics P, Stanley KO (2011) Constraining connectivity to encourage modularity in hyperNEAT. Gecco-2011: proceedings of the 13th annual genetic and evolutionary computation conference, pp 1483–1490
Warren DE, Power JD, Bruss J, Denburg NL, Waldron EJ, Sun H, Petersen SE, Tranel D (2014) Network measures predict neuropsychological outcome after brain injury. Proc Natl Acad Sci USA 111(39):14247–14252. doi:10.1073/pnas.1322173111
Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442
White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314(1165):1–340
Young MP (1992) Objective analysis of the topological organization of the primate cortical visual system. Nature 358(6382):152–155
Zamora-Lopez G, Zhou C, Kurths J (2010) Cortical hubs form a module for multisensory integration on top of the hierarchy of cortical networks. Front Neuroinform 4:1. doi:10.3389/neuro.11.001.2010
Zubler F, Douglas R (2009) A framework for modeling the growth and development of neurons and networks. Front Comput Neurosci 3:25. doi:10.3389/neuro.10.025.2009
Acknowledgments
This work was supported by the Engineering and Physical Sciences Research Council of the United Kingdom (EP/K026992/1) as part of the Human Brain Development Project (http://www.greenbrainproject.org). R.B. was also supported by the Medical Research Council of the United Kingdom (MR/N015037/1).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer Japan KK
About this chapter
Cite this chapter
Bauer, R., Kaiser, M. (2017). Organisational Principles of Connectomes: Changes During Evolution and Development. In: Shigeno, S., Murakami, Y., Nomura, T. (eds) Brain Evolution by Design. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56469-0_17
Download citation
DOI: https://doi.org/10.1007/978-4-431-56469-0_17
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-56467-6
Online ISBN: 978-4-431-56469-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)