Wiring optimization can relate neuronal structure and function.

We pursue the hypothesis that neuronal placement in animals minimizes wiring costs for given functional constraints, as specified by synaptic connectivity. Using a newly compiled version of the Caenorhabditis elegans wiring diagram, we solve for the optimal layout of 279 nonpharyngeal neurons. In the optimal layout, most neurons are located close to their actual positions, suggesting that wiring minimization is an important factor. Yet some neurons exhibit strong deviations from "optimal" position. We propose that biological factors relating to axonal guidance and command neuron functions contribute to these deviations. We capture these factors by proposing a modified wiring cost function.

[1]  The Upper Colorado , 1877, Nature.

[2]  S. Cajal,et al.  Histology of the Nervous System , 1911 .

[3]  MULTIPLE FACTORS IN HEREDITY. , 1914, Science.

[4]  W. Rushton.  A theory of the effects of fibre size in medullated nerve , 1951, The Journal of physiology.

[5]  Kenneth M. Hall.  An r-Dimensional Quadratic Placement Algorithm , 1970 .

[6]  W. Precht.  The synaptic organization of the brain G.M. Shepherd, Oxford University Press (1975). 364 pp., £3.80 (paperback) , 1976, Neuroscience.

[7]  C. Gilbert,et al.  Laminar patterns of geniculocortical projection in the cat , 1976, Brain Research.

[8]  J. Sulston,et al.  Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. , 1977, Developmental biology.

[9]  D. Bray,et al.  Mechanical tension produced by nerve cells in tissue culture. , 1979, Journal of cell science.

[10]  D Purves,et al.  The relation of postsynaptic geometry to the number of presynaptic axons that innervate autonomic ganglion cells , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  J. Sulston,et al.  The embryonic cell lineage of the nematode Caenorhabditis elegans. , 1983, Developmental biology.

[12]  G. Blasdel,et al.  Termination of afferent axons in macaque striate cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  D Purves,et al.  Geometrical differences among homologous neurons in mammals. , 1985, Science.

[14]  S. Brenner,et al.  The neural circuit for touch sensitivity in Caenorhabditis elegans , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  D. Purves,et al.  Relation of animal size to convergence, divergence, and neuronal number in peripheral sympathetic pathways , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  D. Hall,et al.  Genetics of cell and axon migrations in Caenorhabditis elegans. , 1987, Development.

[18]  R W Rodieck,et al.  Parasol and midget ganglion cells of the primate retina. , 1989, The Journal of comparative neurology.

[19]  B. Boycott,et al.  Horizontal Cells in the Monkey Retina: Cone connections and dendritic network , 1989, The European journal of neuroscience.

[20]  J. M. Smith,et al.  Optimality theory in evolutionary biology , 1990, Nature.

[21]  J. Coyne.  Endless forms most beautiful , 1990, Nature.

[22]  Evaluation of the impact of birth control methods on fertility: the case of Shanghai. , 1991, China population research leads.

[23]  PR Martin,et al.  Rod bipolar cells in the macaque monkey retina: immunoreactivity and connectivity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  G. Mitchison.  Neuronal branching patterns and the economy of cortical wiring , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  D A Agard,et al.  Drosophila gastrulation: analysis of cell shape changes in living embryos by three-dimensional fluorescence microscopy , 2005 .

[26]  R. Tsay,et al.  A unified approach to partitioning and placement (VLSI layout) , 1991 .

[27]  J. White,et al.  Mutations in the Caenorhabditis elegans unc–4 gene alter the synaptic input to ventral cord motor neurons , 1992, Nature.

[28]  W Rall,et al.  Matching dendritic neuron models to experimental data. , 1992, Physiological reviews.

[29]  E. Hedgecock,et al.  Guidance of neuroblast migrations and axonal projections in Caenorhabditis elegans , 1992, Current Opinion in Neurobiology.

[30]  Malcolm P. Young,et al.  Objective analysis of the topological organization of the primate cortical visual system , 1992, Nature.

[31]  B. Pakkenberg,et al.  A quantitative study of the human cerebellum with unbiased stereological techniques , 1992, The Journal of comparative neurology.

[32]  AC Tose.  Cell , 1993, Cell.

[33]  H. Horvitz,et al.  The GABAergic nervous system of Caenorhabditis elegans , 1993, Nature.

[34]  D. Dacey,et al.  Recoverin immunoreactivity in mammalian cone bipolar cells , 1993, Visual Neuroscience.

[35]  J. Culotti,et al.  Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally , 1993, Nature.

[36]  D. Dacey.  The mosaic of midget ganglion cells in the human retina , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  M. Chalfie.  Homeobox genes in Caenorhabditis elegans. , 1993, Current opinion in genetics & development.

[38]  J. Budd,et al.  A numerical analysis of the geniculocortical input to striate cortex in the monkey. , 1994, Cerebral cortex.

[39]  C Cherniak,et al.  Component placement optimization in the brain , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  Heinz Wässle,et al.  Immunocytochemical analysis of bipolar cells in the macaque monkey retina , 1994, The Journal of comparative neurology.

[41]  J. C. Anderson,et al.  Polyneuronal innervation of spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.

[42]  C. Cherniak.  Neural component placement , 1995, Trends in Neurosciences.

[43]  S. R. Wicks,et al.  Integration of mechanosensory stimuli in Caenorhabditis elegans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Young Mp,et al.  Component-placement optimization in the brain. , 1996 .

[45]  E. Callaway,et al.  Contributions of individual layer 6 pyramidal neurons to local circuitry in macaque primary visual cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  A. Mccarthy.  Development , 1996, Current Opinion in Neurobiology.

[47]  G. Riedel.  Function of metabotropic glutamate receptors in learning and memory. , 1996, Trends in neurosciences.

[48]  C. Goodman,et al.  The Molecular Biology of Axon Guidance , 1996, Science.

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

[50]  Kai Zinn,et al.  Regulated neurite tension as a mechanism for determination of neuronal arbor geometries in vivo , 1997, Current Biology.

[51]  D. Riddle.  C. Elegans II , 1998 .

[52]  Rob R. de Ruyter van Steveninck,et al.  The metabolic cost of neural information , 1998, Nature Neuroscience.

[53]  S. Lockery,et al.  Active Currents Regulate Sensitivity and Dynamic Range in C. elegans Neurons , 1998, Neuron.

[54]  J. Culotti,et al.  DCC and netrins. , 1998, Current opinion in cell biology.

[55]  R. W. Rodieck.  The First Steps in Seeing , 1998 .

[56]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[57]  S. Cajal.  Texture of the nervous system of man and the vertebrates , 2000 .

[58]  Dmitri B. Chklovskii,et al.  Wiring Optimization in the Brain , 1999, NIPS.

[59]  Santiago Ramón y Cajal,et al.  Texture of the Nervous System of Man and the Vertebrates , 1999, Springer Vienna.

[60]  E. Hedgecock,et al.  Role of netrin UNC-6 in patterning the longitudinal nerves of Caenorhabditis elegans. , 1999, Journal of neurobiology.

[61]  D. Chklovskii,et al.  Optimal sizes of dendritic and axonal arbors in a topographic projection. , 1999, Journal of neurophysiology.

[62]  D. Chklovskii.  Binocular disparity can explain the orientation of ocular dominance stripes in primate primary visual area (V1) , 2000, Vision Research.

[63]  D. Chklovskii,et al.  A wire length minimization approach to ocular dominance patterns in mammalian visual cortex , 2000 .

[64]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[65]  S. Laughlin,et al.  An Energy Budget for Signaling in the Grey Matter of the Brain , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[66]  B. Dickson.  Molecular Mechanisms of Axon Guidance , 2002, Science.

[67]  D. Hall,et al.  Immunoglobulin-Domain Proteins Required for Maintenance of Ventral Nerve Cord Organization , 2002, Science.

[68]  Vitaly A Klyachko,et al.  Connectivity optimization and the positioning of cortical areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[69]  K. Kaibuchi,et al.  Roles of Rho-family GTPases in cell polarisation and directional migration. , 2003, Current opinion in cell biology.

[70]  Cornelia I. Bargmann,et al.  The Immunoglobulin Superfamily Protein SYG-1 Determines the Location of Specific Synapses in C. elegans , 2003, Cell.

[71]  Raul Cristian Muresan,et al.  Pattern recognition using pulse-coupled neural networks and discrete Fourier transforms , 2003, Neurocomputing.

[72]  Dmitri B Chklovskii,et al.  Synaptic Connectivity and Neuronal Morphology Two Sides of the Same Coin , 2004, Neuron.

[73]  Christopher Cherniak,et al.  Local optimization of neuron arbors , 1992, Biological Cybernetics.

[74]  Dmitri B. Chklovskii,et al.  Exact Solution for the Optimal Neuronal Layout Problem , 2004, Neural Computation.

[75]  D. Chklovskii,et al.  Maps in the brain: what can we learn from them? , 2004, Annual review of neuroscience.

[76]  Yishi Jin,et al.  Genetic analysis of synaptic target recognition and assembly , 2004, Trends in Neurosciences.

[77]  H. Cline,et al.  Synaptogenesis: A Balancing Act between Excitation and Inhibition , 2005, Current Biology.

[78]  Quan Wen,et al.  Segregation of the Brain into Gray and White Matter: A Design Minimizing Conduction Delays , 2005, PLoS Comput. Biol..