Maximization of the connectivity repertoire as a statistical principle governing the shapes of dendritic arbors

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 30, 2009, Pages 12536-12541

  Wen, Quan ^a,e   Stepanyants, Armen ^b   Elston, Guy N ^c   Grosberg, Alexander Y ^d   Chklovskii, Dmitri B ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

^c Centre for Cognitive Neuroscience   (Australia)

^d POLYTECHNIC UNIVERSITY   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

Axons; Entropy; Optimization; Pyramidal cell; Scaling

Indexed keywords

ANIMAL CELL; ARTICLE; BRAIN; CELL FUNCTION; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; ENTROPY; MAMMAL; NERVE CONDUCTION; NERVE FIBER; NONHUMAN; OBSERVATION; PHYSICS; PREDICTION; PRIORITY JOURNAL; PURKINJE CELL; PYRAMIDAL NERVE CELL; RAT; THEORY;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; AXONS; DENDRITES; HAPLORHINI; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; PURKINJE CELLS; PYRAMIDAL CELLS; RATS; SYNAPSES;

MAMMALIA;

EID: 68149170901     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0901530106     Document Type: Article

References (77)

1. Ramón y Cajal S (1899) Texture of the Nervous System of Man and the Vertebrates (Springer, New York).
2. Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387-406.
3. Lubke J, Roth A, Feldmeyer D, Sakmann B (2003) Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. Cereb Cortex 13:1051-1063.
4. Kalisman N, Silberberg G, Markram H (2003) Deriving physical connectivity from neuronal morphology. Biol Cybern 88:210-218.
5. Binzegger T, Douglas RJ, Martin KA (2004) A quantitative map of the circuit of cat primary visual cortex. J Neurosci 24:8441-8453.
6. Braitenberg V, Schüz A (1998) Cortex: Statistics and Geometry of Neuronal Connectivity (Springer, Berlin), 2nd Ed.
7. Stepanyants A, Hof PR, Chklovskii DB (2002) Geometry and structural plasticity of synaptic connectivity. Neuron 34:275-288.
8. Stepanyants A, Chklovskii DB (2005) Neurogeometry and potential synaptic connectivity. Trends Neurosci 28:387-394.
9. Uttley AM (1955) The probability of neural connexions. Proc R Soc London Ser B 144:229-240.
10. Spruston N (2008) Pyramidal neurons: Dendritic structure and synaptic integration. Nat Rev Neurosci 9:206-221.
11. Fiala JC, Harris KM (1999) Dendritic structure. Dendrites, eds Stuart G, Spruston N, Häusser M (Oxford Univ Press, New York), 1st Ed, pp 1-34.
12. Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363-366.
13. Haüsser M, Mel B (2003) Dendrites: Bug or feature? Curr Opin Neurobiol 13:372-383.
14. Poirazi P, Mel BW (2001) Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29:779-796.
15. Koch C, Segev I (2000) The role of single neurons in information processing. Nat Neurosci 3(Suppl):1171-1177.
16. DeFelipe J, Farinas I (1992) The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol 39:563-607.
17. Elston GN (2007) Specializations in pyramidal cell structure during primate evolution. Evolution of Nervous Systems, eds Kaas JH, Preuss TM (Academic, Oxford), Vol 4, pp 191-242.
18. Jacobs B, Scheibel AB (2002) Regional dendritic variation in primate cortical pyramidal cells. Cortical Areas: Unity and Diversity, eds Schüz A, Miller R (Taylor and Francis, London), pp 111-131.
19. Elston GN, Rosa MG (1997) The occipitoparietal pathway of the macaque monkey: Comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex 7:432-452.
20. Cherniak C (1992) Local optimization of neuron arbors. Biol Cybern 66:503-510.
21. Chen BL, Hall DH, Chklovskii DB (2006) Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci USA 103:4723-4728.
22. Chklovskii DB (2004) Synaptic connectivity and neuronal morphology: Two sides of the same coin. Neuron 43:609-617.
23. Mitchison G (1991) Neuronal branching patterns and the economy of cortical wiring. Proc Biol Sci 245:151-158.
24. Laughlin SB, Sejnowski TJ (2003) Communication in neuronal networks. Science 301:1870-1874.
25. Kisvarday ZF, Eysel UT (1992) Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17). Neuroscience 46:275-286.
26. Shepherd GM, Svoboda K (2005) Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J Neurosci 25:5670-5679.
27. Smith TG, Jr, Marks WB, Lange GD, Sheriff WH, Jr, Neale EA (1989) A fractal analysis of cell images. J Neurosci Methods 27:173-180.
28. Jelinek H, Elston GN, Zietsch B (2005) Fractal analysis: Pitfalls and revelations in neuroscience. Fractals in Biology and Medicine, eds Losa GA, Merlini D, Non-nenmacher TF, Weibel ER (Birkhauser, Basel), Vol 4, pp 85-94.
29. Caserta F, et al. (1990) Physical mechanisms underlying neurite outgrowth: A quantitative analysis of neuronal shape. Phys Rev Lett 64:95-98.
30. Rothnie P, Kabaso D, Hof PR, Henry BI, Wearne SL (2006) Functionally relevant measures of spatial complexity in neuronal dendritic arbors. J Theor Biol 238:505-526.
31. Jelinek HF, Fernandez E (1998) Neurons and fractals: How reliable and useful are calculations of fractal dimensions? J Neurosci Methods 81:9-18.
32. Milosevic NT, Ristanovic D, Stankovic JB (2005) Fractal analysis of the laminar organization of spinal cord neurons. J Neurosci Methods 146:198-204.
33. Markram H, Lubke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol (London) 500:409-440.
34. Thomson AM, Bannister AP (2003) Interlaminar connections in the neocortex. Cereb Cortex 13:5-14.
35. Sjostrom PJ, Turrigiano GG, Nelson SB (2001) Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32:1149-1164.
36. Trachtenberg JT, et al. (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420:788-794.
37. Gutin AM, Grosberg AY, Shakhnovich EI (1993) Polymers with annealed and quenched branchings belong to different universality classes. Macromolecules 26:1293-1295.
38. Rubinstein M, Colby RH (2003) Polymer Physics (Oxford Univ Press, New York).
39. Magee JC, Cook EP (2000) Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 3:895-903.
40. Chklovskii DB, Mel BW, Svoboda K (2004) Cortical rewiring and information storage. Nature 431:782-788.
41. Cash S, Yuste R (1999) Linear summation of excitatory inputs by CA1 pyramidal neurons. Neuron 22:383-394.
42. Nevian T, Larkum ME, Polsky A, Schiller J (2007) Properties of basal dendrites of layer 5 pyramidal neurons: A direct patch-clamp recording study. Nat Neurosci 10:206-214.
43. Binzegger T, Douglas RJ, Martin KA (2005) Axons in cat visual cortex are topologically self-similar. Cereb Cortex 15:152-165.
44. Kawaguchi Y, Karube F, Kubota Y (2006) Dendritic branch typing and spine expression patterns in cortical nonpyramidal cells. Cereb Cortex 16:696-711.
45. 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.
46. Stepanyants A, Tamas G, Chklovskii DB (2004) Class-specific features of neuronal wiring. Neuron 43:251-259.
47. Cuntz H, Borst A, Segev I (2007) Optimization principles of dendritic structure. Theor Biol Med Model 4:21-28.
48. Burke RE, Marks WB (2002) Some approaches to quantitative dendritic morphology. Computational Neuroanatomy: Principles and Methods, ed Ascoli GA (Humana, Clifton, NJ), p 476.
49. Wen Q, Chklovskii DB (2008) A cost-benefit analysis of neuronal morphology. J Neurophysiol 99:2320-2328.
50. Llinás RR, Walton KD, Lang EJ (2004) Cerebellum. The Synaptic Organization of the Brain, ed Shepherd GM (Oxford Univ Press, New York), 5th Ed, pp 271-309.
51. Losonczy A, Magee JC (2006) Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50:291-307.
52. Poirazi P, Brannon T, Mel BW (2003) Pyramidal neuron as two-layer neural network. Neuron 37:989-999.
53. Poirazi P, Brannon T, Mel BW (2003) Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37:977-987.
54. Nicol D, Meinertzhagen IA (1982) An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly. J Comp Neurol 207:29-44.
55. Gilbert CD, Wiesel TN (1989) Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J Neurosci 9:2432-2442.
56. Mooser F, Bosking WH, Fitzpatrick D (2004) A morphological basis for orientation tuning in primary visual cortex. Nat Neurosci 7:872-879.
57. Fujita I, Fujita T (1996) Intrinsic connections in the macaque inferior temporal cortex. J Comp Neurol 368:467-486.
58. Lund JS, Yoshioka T, Levitt JB (1993) Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cereb Cortex 3:148-162.
59. Anderson JC, Binzegger T, Douglas RJ, Martin KA (2002) Chance or design? Some specific considerations concerning synaptic boutons in cat visual cortex. J Neurocytol 31:211-229.
60. Silver RA, Lubke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302:1981-1984.
61. Stepanyants A, Martinez LM, Ferecsko AS, Kisvarday ZF (2009) The fractions of shortand long-range connections in the visual cortex. Proc Natl Acad Sci USA 106:3555-3560.
62. Hattori D, et al. (2007) Dscam diversity is essential for neuronal wiring and selfrecognition. Nature 449:223-227.
63. Schmucker D, et al. (2000) Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671-684.
64. Hughes ME, et al. (2007) Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54:417-427.
65. Fuerst PG, Koizumi A, Masland RH, Burgess RW (2008) Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451:470-474.
66. Yamagata M, Sanes JR (2008) Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451:465-469.
67. Samsonovich AV, Ascoli GA (2005) Statistical determinants of dendritic morphology in hippocampal pyramidal neurons: A hidden Markov model. Hippocampus 15:166-183.
68. van Pelt J, Uylings HB (2002) Branching rates and growth functions in the outgrowth of dendritic branching patterns. Network 13:261-281.
69. Sugimura K, Shimono K, Uemura T, Mochizuki (2007) A self-organizing mechanism for development of space-filling neuronal dendrites. PLoS Comput Biol 3:e212.
70. Marks WB, Burke RE (2007) Simulation of motoneuron morphology in three dimensions. I. Building individual dendritic trees. J Comp Neurol 503:685-700.
71. Marks WB, Burke RE (2007) Simulation of motoneuron morphology in three dimensions. II. Building complete neurons. J Comp Neurol 503:701-716.
72. Mauseth JD (2003) Botany: An Introduction to Plant Biology (Jones and Bartlett, Boston), 3rd Ed.
73. Thomas PA (2001) Trees: Their Natural History (Cambridge Univ Press, Cambridge, UK), 1st Ed.
74. Ascoli GA (2006) Mobilizing the base of neuroscience data: The case of neuronal morphologies. Nat Rev Neurosci 7:318-324.
75. Martone ME, et al. (2003) The cell-centered database: A database for multiscale structural and protein localization data from light and electron microscopy. Neuroinformatics 1:379-395.
76. Rapp M, Segev I, Yarom Y (1994) Physiology, morphology and detailed passive models of guinea-pig cerebellar Purkinje cells. J Physiol (London) 474:101-118.
77. Vetter P, Roth A, Hausser M (2001) Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol 85:926-937.