A simple rule for axon outgrowth and synaptic competition generates realistic connection lengths and filling fractions

Cerebral Cortex

Volumn 19, Issue 12, 2009, Pages 3001-3010

  Kaiser, Marcus ^a,b   Hilgetag, Claus C ^c,d   Van Ooyen, Arjen ^e  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c JACOBS UNIVERSITY BREMEN   (Germany)

^d BOSTON UNIVERSITY   (United States)

^e VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Axon growth; Cortical networks; Filling fraction; Neural competition; Neural networks

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CAENORHABDITIS ELEGANS; CELL POPULATION; CELL SIZE; CONTROLLED STUDY; HUMAN; MACACA; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC POTENTIAL; VISUAL CORTEX;

ANIMALS; AXONS; CELL ENLARGEMENT; COMPUTER SIMULATION; MACACA; MODELS, ANATOMIC; MODELS, NEUROLOGICAL; MORPHOGENESIS; SYNAPSES;

EID: 70450237135     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp071     Document Type: Article

References (62)

1. Achacoso TB, Yamamoto WS. 1992. AY's neuroanatomy of C. elegans for computation. Boca Raton (FL): CRC Press
2. Amirikian B. 2005. A phenomenological theory of spatially structured local synaptic connectivity. PLoS Comput Biol. 1:e11
3. Baruch L, Itzkovitz S, Golan-Mashiach M, Shapiro E, Segal E. 2008. Using expression profiles of Caenorhabditis elegans neurons to identify genes that mediate synaptic connectivity. PLoS Comput Biol. 4:e1000120
4. Binzegger T, Douglas RJ, Martin KAC. 2004. A quantitative map of the circuit of cat primary visual cortex. J Neurosci. 24:8441-8453
5. Borisyuk R, Cooke T, Roberts A. 2008. Stochasticity and functionality of neural systems: mathematical modelling of axon growth in the spinal cord of tadpole. Biosystems. 93:101-114
6. Braitenberg V, Schuez A. 1998. Cortex: statistics and geometry of neuronal connectivity. Heidelberg: Springer
7. Butz M, Worgotter F, Van Ooyen A. 2009. Activity-dependent structural plasticity. Brain Res Rev. Forthcoming
8. Cabelli RJ, Hohn A, Shatz CJ. 1995. Inhibition of ocular dominance column formation by infusion of Nt-4/5 or Bdnf. Science. 267:1662-1666
9. Carmichael ST, Price JL. 1994. Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol. 346:366-402
10. Chklovskii DB. 2004. Exact solution for the optimal neuronal layout problem. Neural Comput. 16:2067-2078
11. Choe Y, McCormcik BH, Koh W. 2004. Network connectivity analysis on the temporally augmented C. elegans web: a pilot study. Soc Neurosci Abstr. 30:921-929
12. Costa LdF, Kaiser M, Hilgetag CC. 2007. Predicting the connectivity of primate cortical networks from topological and spatial node properties. BMC Syst Biol. 1:16
13. Costa LdF, Rodrigues FA, Travieso G, Villas Boas PR. 2007. Characterization of complex networks: a survey of measurements. Adv Phys. 56:167-242
14. Crepel F. 1982. Regression of functional synapses in the immature mammalian cerebellum. Trends Neurosci. 5:266-269
15. Easter SS Jr, Purves D, Rakic P, Spitzer NC. 1985. The changing view of neural specificity. Science. 230:507-511
16. Felleman DJ, van Essen DC. 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex. 1:1-47
17. Hellwig B. 2000. A quantitative analysis of the local connectivity between pyramidal neurons in layers 2/3 of the rat visual cortex. Biol Cybern. 82:111-121
18. Hellwig B, Schuz A, Aertsen A. 1994. Synapses on axon collaterals of pyramidal cells are spaced at random intervals: a Golgi study in the mouse cerebral cortex. Biol Cybern. 71:1-12
19. Hilgetag CC, Burns GAPC, O'Neill MA, Scannell JW, Young MP. 2000. Anatomical connectivity defines the organization of clusters of cortical areas in the macaque monkey and the cat. Phil Trans R Soc Lond B. 355:91-110
20. Hume RI, Purves D. 1981. Geometry of neonatal neurones and the regulation of synapse elimination. Nature. 293:469-471
21. Kaiser M, Hilgetag CC. 2004. Modelling the development of cortical networks. Neurocomputing. 58-60:297-302
22. Kaiser M, Hilgetag CC. 2006. Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol. 2:e95
23. Kaiser M, Hilgetag CC. 2007. Development of multi-cluster cortical networks by time windows for spatial growth. Neurocomputing. 70:1829-1832 (Pubitemid 46656970)
24. Kaiser M, Martin R, Andras P, Young MP. 2007. Simulation of robustness against lesions of cortical networks. Eur J Neurosci. 25:3185-3192
25. Kalisman N, Silberberg G, Markram H. 2005. The neocortical microcircuit as a tabula rasa. Proc Natl Acad Sci USA. 102:880-885
26. Kaufman A, Dror G, Meilijson I, Ruppin E. 2006. Gene expression of C. elegans neurons carries information on their synaptic connectivity. PLoS Comput Biol. 2:e167
27. Kisvarday ZF, Martin KA, Freund TF, Magloczky Z, Whitteridge D, Somogyi P. 1986. Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex. Exp Brain Res. 64:541-552
28. Kotter R. 2004. Online retrieval, processing, and visualization of primate connectivity data from the CoCoMac database. Neuroinformatics. 2:127-144
29. LaMantia AS, Rakic P. 1990. Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey. J Neurosci. 10:2156-2175
30. Lewis JW, Essen DCV. 2000. Architectonic parcellation of parieto-occipital cortex and interconnected cortical regions in the macaque monkey. J Comp Neurol. 428:79-111
31. Lohmann H, Rorig B. 1994. Long-range horizontal connections between supragranular pyramidal cells in the extrastriate visual cortex of the rat. J Comp Neurol. 344:543-558
32. Lohof AM, DelhayeBouchaud N, Mariani J. 1996. Synapse elimination in the central nervous system: functional significance and cellular mechanisms. Rev Neurosci. 7:85-101
33. McGuire BA, Gilbert CD, Rivlin PK, Wiesel TN. 1991. Targets of horizontal connections in macaque primary visual cortex. J Comp Neurol. 305:370-392
34. Murray JD. 1990. Mathematical biology. Heidelberg: Springer
35. Nisbach F, Kaiser M. 2007. Time domains for spatial network development generate multiple-cluster small-world networks. Eur Phys J B. 58:185-191
36. Purves D, Lichtman JW. 1980. Elimination of synapses in the developing nervous system. Science. 210:153-157
37. Rakic P. 1981. Development ofvisual centers in the primate brain depends on binocular competition before birth. Science. 214:928-931
38. Rakic P. 1986. Mechanism of ocular dominance segregation in the lateral geniculate nucleus: competitive elimination hypothesis. Trends Neurosci. 9:11-15
39. Rakic P. 2002. Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat Rev Neurosci. 3:65-71
40. Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS. 1986. Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science. 232:232-235
41. Rakic P, Riley KP. 1983. Overproduction and elimination of retinal axons in the fetal rhesus monkey. Science. 219:1441-1444
42. Samsonovich AV, Ascoli GA. 2003. Statistical morphological analysis of hippocampal principal neurons indicates cell-specific repulsion of dendrites from their own cell. J Neurosci Res. 71:173-187
43. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci. 22:389-442
44. Sperry RW. 1963. Chemoaffinity in the orderly growth of nerve fiber pattern and connections. Proc Natl Acad Sci USA. 50:703-710
45. Sporns O, Chialvo DR, Kaiser M, Hilgetag CC. 2004. Organization, development and function of complex brain networks. Trends Cogn Sci. 8:418-425
46. Stepanyants A, Hof PR, Chklovskii DB. 2002. Geometry and structural plasticity of synaptic connectivity. Neuron. 34:275-288
47. Stephan KE, Kamper L, Bozkurt A, Burns GA, Young MP, Kotter R. 2001. Advanced database methodology for the Collation of connectivity data on the macaque brain (CoCoMac). Philos Trans R Soc Lond B Biol Sci. 356:1159-1186
48. Stephan KE, Zilles K, Kotter R. 2000. Coordinate-independent mapping of structural and functional data by objective relational transformation (ORT). Philos Trans R Soc Lond B Biol Sci. 355:37-54
49. Tarui T, Takahashi T, Nowakowski RS, Hayes NL, Bhide PG, Caviness VS. 2005. Overexpression of p27(Kip1), probability of cell cycle exit, and laminar destination of neocortical neurons. Cereb Cortex. 15:1343-1355
50. Uylings HB, van Pelt J. 2002. Measures for quantifying dendritic arborizations. Network. 13:397-414
51. van Ooyen A. 2001. Competition in the development of nerve connections: a review of models. Network. 12:R1-R47
52. van Ooyen A. 2003. Modeling neural development. Cambridge, MA: MIT Press
53. van Ooyen A. 2005. Competition in neurite outgrowth and the development of nerve connections. Prog Brain Res. 147:81-99
54. van Ooyen A, Van Pelt J, Corner MA. 1995. Implications of activity dependent neurite outgrowth for neuronal morphology and network development. J Theor Biol. 172:63-82
55. van Ooyen A, Willshaw DJ. 1999. Competition for neurotrophic factor in the development of nerve connections. Proc Biol Sci. 266:883-892
56. van Ooyen A, Willshaw DJ, Ramakers GJA. 2000. Influence of dendritic morphology on axonal competition. Neurocomputing. 32:255-260
57. Verhage M, Maia AS, Plomp JJ, Brussaard AB, Heeroma JH, Vermeer H, Toonen RF, Hammer RE, van den Berg TK, Missler M, et al. 2000. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science. 287:864-869
58. Watts DJ, Strogatz SH. 1998. Collective dynamics of 'small-world' networks. Nature. 393:440-442
59. Wen Q, Chklovskii DB. 2008. A cost-benefit analysis of neuronal morphology. J Neurophysiol. 99:2320-2328
60. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode C. elegans. Phil Trans R Soc of London B. 314:1
61. Wiesel TN. 1982. Postnatal-development of the visual-cortex and the influence of environment. Nature. 299:583-591
62. Yamamoto N, Tamada A, Murakami F. 2002. Wiring of the brain by a range of guidance cues. Prog Neurobiol. 68:393-407