Deterministic and stochastic elements of axonal guidance.

An enormous literature has been developed on investigations of the growth and guidance of axons during development and after injury. In this review, we provide a guide to this literature as a resource for biomedical investigators. We first review briefly the molecular biology that is known to regulate migration of the growth cone and branching of axonal arbors. We then outline some important fundamental considerations that are important to the modeling of the phenomenology of these guidance effects and of what is known of their underlying internal mechanisms. We conclude by providing some thoughts on the outlook for future biomedical modeling in the field.

[1]  Julie H. Simpson,et al.  Short-Range and Long-Range Guidance by Slit and Its Robo Receptors Robo and Robo2 Play Distinct Roles in Midline Guidance , 2000, Neuron.

[2]  H. Buettner Computer simulation of nerve growth cone filopodial dynamics for visualization and analysis. , 1995, Cell motility and the cytoskeleton.

[3]  H. Berg,et al.  Physics of chemoreception. , 1977, Biophysical journal.

[4]  T. Hunter,et al.  EphrinA1-induced cytoskeletal re-organization requires FAK and p130cas , 2002, Nature Cell Biology.

[5]  James Q. Zheng Turning of nerve growth cones induced by localized increases in intracellular calcium ions , 2000, Nature.

[6]  C Blakemore,et al.  Morphology and Growth Patterns of Developing Thalamocortical Axons , 2000, The Journal of Neuroscience.

[7]  G. Edelman,et al.  Structure of a new nervous system glycoprotein, Nr-CAM, and its relationship to subgroups of neural cell adhesion molecules , 1991, The Journal of cell biology.

[8]  Marc Tessier-Lavigne,et al.  Roundabout Controls Axon Crossing of the CNS Midline and Defines a Novel Subfamily of Evolutionarily Conserved Guidance Receptors , 1998, Cell.

[9]  Marc Tessier-Lavigne,et al.  Conservation and divergence of axon guidance mechanisms , 1999, Current Opinion in Neurobiology.

[10]  Mu-ming Poo,et al.  cAMP-induced switching in turning direction of nerve growth cones , 1997, Nature.

[11]  R. W. Gundersen,et al.  Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectin in vitro. , 1987, Developmental biology.

[12]  K W Tosney,et al.  Identification of an Invariant Response: Stable Contact with Schwann Cells Induces Veil Extension in Sensory Growth Cones , 2000, The Journal of Neuroscience.

[13]  S. J. Smith,et al.  Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone , 1988, The Journal of cell biology.

[14]  D. Lauffenburger Cell signaling pathways as control modules: complexity for simplicity? , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Pelt Effect of pruning on dendritic tree topology. , 1997 .

[16]  A. Carriquiry,et al.  Mathematical modeling of dendritic growth in vitro , 1995, Brain Research.

[17]  E. B. George,et al.  Axonal elongation as a stochastic walk. , 1984, Cell motility.

[18]  Michael D. Kim,et al.  Growth Cone Pathfinding and Filopodial Dynamics Are Mediated Separately by Cdc42 Activation , 2002, The Journal of Neuroscience.

[19]  D Kleinfeld,et al.  Controlled outgrowth of dissociated neurons on patterned substrates , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Geoffrey B. West,et al.  Scaling in Biology , 2000 .

[21]  G. Goodhill,et al.  Theoretical analysis of gradient detection by growth cones. , 1999, Journal of neurobiology.

[22]  J. Silver,et al.  Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro , 1990, Experimental Neurology.

[23]  J. Challacombe,et al.  Actin filament bundles are required for microtubule reorientation during growth cone turning to avoid an inhibitory guidance cue. , 1996, Journal of cell science.

[24]  P. Camilli,et al.  Glutamate regulates actin-based motility in axonal filopodia , 2001, Nature Neuroscience.

[25]  M. Kirschner,et al.  Microtubule behavior in the growth cones of living neurons during axon elongation , 1991, The Journal of cell biology.

[26]  T. Shinbrot,et al.  A chaotic attractor in timing noise from the Vela pulsar , 1990 .

[27]  A. Kolodkin,et al.  Semaphorin junction: making tracks toward neural connectivity , 2003, Current Opinion in Neurobiology.

[28]  D. Bentley,et al.  Pioneer growth cone steering along a series of neuronal and non- neuronal cues of different affinities , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  M. VanBerkum,et al.  Regulation of rho family GTPases is required to prevent axons from crossing the midline. , 2002, Developmental biology.

[30]  Bruce P. Graham,et al.  Competition for tubulin between growing neurites during development , 2001, Neurocomputing.

[31]  E. Hazum,et al.  Biotinylated Endothelin Analogs as Probes for Endothelin Receptor , 1993 .

[32]  T. McLaughlin,et al.  Topographic-Specific Axon Branching Controlled by Ephrin-As Is the Critical Event in Retinotectal Map Development , 2001, The Journal of Neuroscience.

[33]  Yi Rao,et al.  Distinguishing between Directional Guidance and Motility Regulation in Neuronal Migration , 2003, The Journal of Neuroscience.

[34]  M. Schwab,et al.  Regeneration of Lesioned Corticospinal Tract Fibers in the Adult Rat Induced by a Recombinant, Humanized IN-1 Antibody Fragment , 2000, The Journal of Neuroscience.

[35]  D. Snow,et al.  Fibronectin and laminin elicit differential behaviors from SH‐SY5Y growth cones contacting inhibitory chondroitin sulfate proteoglycans , 2001, Journal of neuroscience research.

[36]  C E Holt,et al.  A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  Alexander E. Dityatev,et al.  Natural variability in the number of dendritic segments: Model‐based inferences about branching during neurite outgrowth , 1997, The Journal of comparative neurology.

[38]  R E Burke,et al.  A parsimonious description of motoneuron dendritic morphology using computer simulation , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  B. Key,et al.  Multiple axon guidance cues establish the olfactory topographic map: how do these cues interact? , 2002, The International journal of developmental biology.

[40]  P Z Myers,et al.  Growth cone dynamics during the migration of an identified commissural growth cone , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  M. Kirschner,et al.  Microtubule behavior during guidance of pioneer neuron growth cones in situ , 1991, The Journal of cell biology.

[42]  The trappist's approach to pathfinding: elucidating brain wiring using secretory-trap mutagenesis , 2001, Genome Biology.

[43]  K. Kalil,et al.  Interstitial Branches Develop from Active Regions of the Axon Demarcated by the Primary Growth Cone during Pausing Behaviors , 1998, The Journal of Neuroscience.

[44]  Y. Rao,et al.  Signalling mechanisms mediating neuronal responses to guidance cues , 2003, Nature Reviews Neuroscience.

[45]  R. Morimoto,et al.  Bag1–Hsp70 mediates a physiological stress signalling pathway that regulates Raf-1/ERK and cell growth , 2001, Nature Cell Biology.

[46]  T. Gómez,et al.  Filopodia initiate choices made by sensory neuron growth cones at laminin/fibronectin borders in vitro , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  Jonathan Grimes,et al.  The Crystal Structure of Plasma Gelsolin: Implications for Actin Severing, Capping, and Nucleation , 1997, Cell.

[48]  Isaac Meilijson,et al.  Neuronal Regulation: A Mechanism for Synaptic Pruning During Brain Maturation , 1999, Neural Computation.

[49]  Leah Edelstein-Keshet,et al.  Regulation of actin dynamics in rapidly moving cells: a quantitative analysis. , 2002, Biophysical journal.

[50]  M. Kirschner,et al.  The role of microtubule dynamics in growth cone motility and axonal growth , 1995, The Journal of cell biology.

[51]  A. Provenzale,et al.  Finite correlation dimension for stochastic systems with power-law spectra , 1989 .

[52]  C. Holt,et al.  Navigational errors made by growth cones without filopodia in the embryonic xenopus brain , 1993, Neuron.

[53]  C. Holt,et al.  Retinal axon guidance: novel mechanisms for steering , 2004, Current Opinion in Neurobiology.

[54]  J. Fawcett,et al.  Report of International Clinical Trials Workshop on Spinal Cord Injury February 20–21, 2004, Vancouver, Canada , 2004, Spinal Cord.

[55]  E. Dent,et al.  Cytoskeletal Dynamics and Transport in Growth Cone Motility and Axon Guidance , 2003, Neuron.

[56]  Dunn Ga,et al.  Characterising a kinesis response: time averaged measures of cell speed and directional persistence. , 1983 .

[57]  R. Macnab Bacterial flagella rotating in bundles: a study in helical geometry. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[58]  G. Fishell,et al.  Radial Glial Cell Line C6-R Integrates Preferentially in Adult White Matter and Facilitates Migration of Coimplanted Neurons in Vivo , 2001, Experimental Neurology.

[59]  W. Sossin,et al.  Protein Kinase C Activation Promotes Microtubule Advance in Neuronal Growth Cones by Increasing Average Microtubule Growth Lifetimes , 2001, The Journal of cell biology.

[60]  C. Cohan,et al.  Focal loss of actin bundles causes microtubule redistribution and growth cone turning , 2002, The Journal of cell biology.

[61]  Julie H. Simpson,et al.  Short-Range and Long-Range Guidance by Slit and Its Robo Receptors A Combinatorial Code of Robo Receptors Controls Lateral Position , 2000, Cell.

[62]  C. Masson,et al.  Statistical analysis and parsimonious modelling of dendrograms of in vitro neurones , 2000, Bulletin of mathematical biology.

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

[64]  C. Mason,et al.  Retinal axon divergence in the optic chiasm: dynamics of growth cone behavior at the midline [published erratum appears in J Neurosci 1995 Mar;15(3):following table of contents] , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  A. D. Kaiser,et al.  Spatial control of cell differentiation in Myxococcus xanthus. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Mu-ming Poo,et al.  Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1 , 1999, Nature.

[67]  Chi-Bin Chien,et al.  Pathfinding and Error Correction by Retinal Axons The Role of astray/robo2 , 2002, Neuron.

[68]  Stephen G. Brush,et al.  Nineteenth-Century Physics. (Book Reviews: The Kind of Motion We Call Heat. A History of the Kinetic Theory of Gases in the 19th Century) , 1978 .

[69]  L. Greene,et al.  Growth cone configuration and advance: a time-lapse study using video- enhanced differential interference contrast microscopy , 1988, Journal of Neuroscience.

[70]  N. L. Hayes,et al.  Competitive interactions during dendritic growth: a simple stochastic growth algorithm , 1992, Brain Research.

[71]  C. Mason,et al.  Growth Cone Form Is Behavior-Specific and, Consequently, Position-Specific along the Retinal Axon Pathway , 1997, The Journal of Neuroscience.

[72]  G. Goodhill Diffusion in Axon Guidance , 1997, The European journal of neuroscience.

[73]  R. Yuste,et al.  Stereotyped position of local synaptic targets in neocortex. , 2001, Science.

[74]  James Q. Zheng,et al.  cAMP-Mediated Regulation of Neurotrophin-Induced Collapse of Nerve Growth Cones , 1998, The Journal of Neuroscience.

[75]  A. Hall,et al.  The Activity of the Plexin-A1 Receptor Is Regulated by Rac* , 2004, Journal of Biological Chemistry.

[76]  J. Goldberg How does an axon grow? , 2003, Genes & development.

[77]  Uwe Drescher,et al.  Ephrin-As as receptors in topographic projections , 2002, Trends in Neurosciences.

[78]  Geoffrey J. Goodhill,et al.  A Theoretical Model of Axon Guidance by the Robo Code , 2003, Neural Computation.

[79]  D. Bentley,et al.  Pioneer growth cone behavior at a differentiating limb segment boundary in the grasshopper embryo. , 1987, Developmental biology.

[80]  B. Tang Inhibitors of neuronal regeneration: mediators and signaling mechanisms , 2003, Neurochemistry International.

[81]  B. Dickson,et al.  Crossing the Midline Roles and Regulation of Robo Receptors , 2000, Neuron.

[82]  A. B. Huber,et al.  Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. , 2003, Annual review of neuroscience.

[83]  K. Kalil,et al.  Common mechanisms underlying growth cone guidance and axon branching. , 2000, Journal of neurobiology.

[84]  P. Bovolenta,et al.  Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[85]  Claire Russell,et al.  Dosage-Sensitive and Complementary Functions of Roundabout and Commissureless Control Axon Crossing of the CNS Midline , 1998, Neuron.

[86]  Jonathan A Raper,et al.  Semaphorins and their receptors in vertebrates and invertebrates , 2000, Current Opinion in Neurobiology.

[87]  William H. Press,et al.  Numerical recipes in C. The art of scientific computing , 1987 .

[88]  James Q. Zheng,et al.  Growth Cone Turning Induced by Direct Local Modification of Microtubule Dynamics , 2002, The Journal of Neuroscience.

[89]  Gianluca Gallo,et al.  Regulation of growth cone actin filaments by guidance cues. , 2004, Journal of neurobiology.

[90]  P. Gordon-Weeks Evidence for microtubule capture by filopodial actin filaments in growth cones. , 1991, Neuroreport.

[91]  P C Letourneau,et al.  Neurite extension across regions of low cell-substratum adhesivity: implications for the guidepost hypothesis of axonal pathfinding. , 1986, Developmental biology.

[92]  K. Aktories,et al.  Rac1 and Cdc42 but Not RhoA or Rho Kinase Activities Are Required for Neurite Outgrowth Induced by the Netrin-1 Receptor DCC (Deleted in Colorectal Cancer) in N1E-115 Neuroblastoma Cells* , 2002, The Journal of Biological Chemistry.

[93]  B. Mueller,et al.  Growth cone guidance: first steps towards a deeper understanding. , 1999, Annual review of neuroscience.

[94]  William H. Press,et al.  The Art of Scientific Computing Second Edition , 1998 .

[95]  Eshel Ben-Jacob,et al.  The artistry of nature , 2001, Nature.

[96]  S. Skaper,et al.  Cell signalling cascades regulating neuronal growth-promoting and inhibitory cues , 2001, Progress in Neurobiology.

[97]  S. B. Kater,et al.  Stimulus History Alters Behavioral Responses of Neuronal Growth Cones , 2000, The Journal of Neuroscience.

[98]  H. Baier,et al.  Zebrafish mutations affecting retinotectal axon pathfinding. , 1996, Development.

[99]  Mu-ming Poo,et al.  Adaptation in the chemotactic guidance of nerve growth cones , 2002, Nature.

[100]  D. Bray,et al.  Analysis of microspike movements on the neuronal growth cone , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[101]  Rüdiger Klein,et al.  Axon guidance: receptor complexes and signaling mechanisms , 2002, Current Opinion in Neurobiology.

[102]  P Connolly,et al.  Growth cone guidance and neuron morphology on micropatterned laminin surfaces. , 1993, Journal of cell science.

[103]  H. R. Payne,et al.  Modulation of growth cone morphology by substrate-bound adhesion molecules. , 1992, Cell motility and the cytoskeleton.

[104]  J. Sweeney,et al.  Computer model: investigating role of filopodia-based steering in experimental neurite galvanotropism. , 1997, Journal of theoretical biology.

[105]  T. Diefenbach,et al.  Modeling the role of myosin 1c in neuronal growth cone turning. , 2003, Biophysical journal.

[106]  L. Landmesser,et al.  Growth cone morphology and trajectory in the lumbosacral region of the chick embryo , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[107]  H. Meinhardt Orientation of chemotactic cells and growth cones: models and mechanisms. , 1999, Journal of cell science.

[108]  Richard B. Dickinson,et al.  Optimal estimation of cell movement indices from the statistical analysis of cell tracking data , 1993 .

[109]  Paul C. Letourneau,et al.  Distribution and possible interactions of actin-associated proteins and cell adhesion molecules of nerve growth cones. , 1989, Development.

[110]  P. Forscher,et al.  Cytoskeletal remodeling during growth cone-target interactions , 1993, The Journal of cell biology.

[111]  M. Schwab,et al.  Sprouting and Regeneration of Lesioned Corticospinal Tract Fibres in the Adult Rat Spinal Cord , 1993, The European journal of neuroscience.

[112]  Eshel Ben-Jacob,et al.  Generic modeling of chemotactic based self-wiring of neural networks , 1998, Neural Networks.

[113]  Christine E Schmidt,et al.  Neural tissue engineering: strategies for repair and regeneration. , 2003, Annual review of biomedical engineering.

[114]  H. Hentschel,et al.  Models of axon guidance and bundling during development , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[115]  E. Feldman,et al.  Signaling mechanisms that regulate actin‐based motility processes in the nervous system , 2002, Journal of neurochemistry.

[116]  Stephen W. Wilson,et al.  N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neurites , 2003, Development.

[117]  James W. Fawcett,et al.  Building a Bridge: Engineering Spinal Cord Repair , 2002, Experimental Neurology.

[118]  P. Forscher,et al.  An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance , 1998, Current Opinion in Neurobiology.

[119]  D. Goldberg,et al.  Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy , 1986, The Journal of cell biology.

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

[121]  Jaap van Pelt,et al.  Neuritic growth rate described by modeling microtubule dynamics , 1994 .

[122]  J. van Pelt,et al.  A model for outgrowth of branching neurites , 1992 .

[123]  E. Kandel Nerve cells and behavior. , 1970, Scientific American.

[124]  Geoffrey J. Goodhill,et al.  Mathematical guidance for axons , 1998, Trends in Neurosciences.

[125]  D. Bentley,et al.  Pioneer growth cone steering decisions mediated by single filopodial contacts in situ , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[126]  Alberto Granato,et al.  Effects of early ethanol exposure on dendrite growth of cortical pyramidal neurons: inferences from a computational model. , 2003, Brain research. Developmental brain research.

[127]  M. Steketee,et al.  Contact with Isolated Sclerotome Cells Steers Sensory Growth Cones by Altering Distinct Elements of Extension , 1999, The Journal of Neuroscience.

[128]  Mu-ming Poo,et al.  Signalling and crosstalk of Rho GTPases in mediating axon guidance , 2003, Nature Cell Biology.

[129]  John Tyler Bonner,et al.  A DESCRIPTIVE STUDY OF THE DEVELOPMENT OF THE SLIME MOLD DICTYOSTELIUM DISCOIDEUM , 1944 .

[130]  G H Li,et al.  On the mechanisms of growth cone locomotion: modeling and computer simulation. , 1994, Journal of theoretical biology.

[131]  H M Buettner,et al.  A model of neurite extension across regions of nonpermissive substrate: simulations based on experimental measurement of growth cone motility and filopodial dynamics. , 1994, Developmental biology.

[132]  C. Holt,et al.  Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: a time-lapse video study of single fibres in vivo. , 1987, Development.

[133]  T. Kennedy,et al.  The Adaptor Protein Nck-1 Couples the Netrin-1 Receptor DCC (Deleted in Colorectal Cancer) to the Activation of the Small GTPase Rac1 through an Atypical Mechanism* , 2002, The Journal of Biological Chemistry.

[134]  M. J. Katz How straight do axons grow? , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[135]  Andreas Schierwagen,et al.  Modeling dendritic morphological complexity of deep layer cat superior colliculus neurons , 2001, Neurocomputing.

[136]  S. Dunnett,et al.  Spatially and temporally restricted chemoattractive and chemorepulsive cues direct the formation of the nigro‐striatal circuit , 2004, The European journal of neuroscience.

[137]  Kathryn W. Tosney,et al.  Contact-mediated mechanisms of motor axon segmentation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[138]  K. Kalil,et al.  Dynamic behaviors of growth cones extending in the corpus callosum of living cortical brain slices observed with video microscopy , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[139]  Philip Ball,et al.  The Self-Made Tapestry: Pattern Formation in Nature , 1999 .

[140]  A. V. Ooyen,et al.  A computational model of dendrite elongation and branching based on MAP2 phosphorylation. , 2001, Journal of theoretical biology.

[141]  D. Bray Protein molecules as computational elements in living cells , 1995, Nature.

[142]  Andreas Schierwagen,et al.  Morphological analysis and modeling of neuronal dendrites. , 2004, Mathematical biosciences.

[143]  A. Koleske Do Filopodia Enable the Growth Cone to Find Its Way? , 2003, Science's STKE.

[144]  P. Bridgman,et al.  Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity , 1992, The Journal of cell biology.

[145]  J. Vanpelt,et al.  Growth cone dynamics and activity-dependent processes in neuronal network development. , 1996 .

[146]  P. Forscher,et al.  Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. , 2000, Journal of neurobiology.

[147]  T D Pollard,et al.  Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. , 2000, Annual review of biophysics and biomolecular structure.

[148]  Herwig Baier,et al.  Axon Guidance: Stretching Gradients to the Limit , 1998, Neural Computation.

[149]  J. Challacombe,et al.  Dynamic Microtubule Ends Are Required for Growth Cone Turning to Avoid an Inhibitory Guidance Cue , 1997, The Journal of Neuroscience.

[150]  R. Lasek,et al.  Early axon patterns of the spinal cord: experiments with a computer. , 1985, Developmental biology.

[151]  S. Leibler,et al.  Robustness in simple biochemical networks , 1997, Nature.

[152]  Paul A Yates,et al.  Computational modeling of retinotopic map development to define contributions of EphA-ephrinA gradients, axon-axon interactions, and patterned activity. , 2004, Journal of neurobiology.

[153]  David G. Wilkinson,et al.  Multiple roles of eph receptors and ephrins in neural development , 2001, Nature Reviews Neuroscience.

[154]  J. Schlessinger,et al.  Induction of Neurite Outgrowth through Contactin and Nr-CAM by Extracellular Regions of Glial Receptor Tyrosine Phosphatase β , 1997, The Journal of cell biology.

[155]  S. Kater,et al.  Regulation of growth cone behavior by calcium , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[156]  Hailan Hu,et al.  Plexin B Mediates Axon Guidance in Drosophila by Simultaneously Inhibiting Active Rac and Enhancing RhoA Signaling , 2001, Neuron.

[157]  T. O'Connor,et al.  Mechanisms of growth cone guidance and motility in the developing grasshopper embryo. , 2000, Journal of neurobiology.

[158]  Mu-ming Poo,et al.  Calcium signalling in the guidance of nerve growth by netrin-1 , 2000, Nature.

[159]  C. Holt,et al.  Apoptotic Pathway and MAPKs Differentially Regulate Chemotropic Responses of Retinal Growth Cones , 2003, Neuron.

[160]  C. Holt,et al.  Chemotropic Responses of Retinal Growth Cones Mediated by Rapid Local Protein Synthesis and Degradation , 2001, Neuron.

[161]  V. Dietz,et al.  Locomotor Recovery in Spinal Cord-Injured Rats Treated with an Antibody Neutralizing the Myelin-Associated Neurite Growth Inhibitor Nogo-A , 2001, The Journal of Neuroscience.

[162]  A. W. Schaefer,et al.  Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones , 2002, The Journal of cell biology.

[163]  M. Spira,et al.  Alteration of Sodium Currents by New Peptide Toxins From the Venom of a Molluscivorous Conus Snail , 1993, The European journal of neuroscience.

[164]  L. Venance,et al.  Control and Plasticity of Intercellular Calcium Waves in Astrocytes: A Modeling Approach , 2002, The Journal of Neuroscience.

[165]  E. Pasquale,et al.  Ephrin-A5 Exerts Positive or Inhibitory Effects on Distinct Subsets of EphA4-Positive Motor Neurons , 2004, The Journal of Neuroscience.

[166]  C. Goodman,et al.  Slit Is the Midline Repellent for the Robo Receptor in Drosophila , 1999, Cell.

[167]  M. Kirschner,et al.  The role of microtubules in growth cone turning at substrate boundaries , 1995, The Journal of cell biology.

[168]  M. Poo,et al.  The cell biology of neuronal navigation , 2001, Nature Cell Biology.

[169]  Kurt Wiesenfeld,et al.  Stochastic resonance and the benefits of noise: from ice ages to crayfish and SQUIDs , 1995, Nature.

[170]  Helen M. Buettner,et al.  Nerve Growth Dynamics , 1994 .

[171]  M. Poo,et al.  Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning , 2003, Nature.

[172]  M. Poo,et al.  Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[173]  D. O'Leary,et al.  Maturation-dependent upregulation of growth-promoting molecules in developing cortical plate controls thalamic and cortical neurite growth , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[174]  Jeffrey L. Krichmar,et al.  Computer generation and quantitative morphometric analysis of virtual neurons , 2001, Anatomy and Embryology.

[175]  Troy Shinbrot,et al.  Growth Cone Pathfinding: a competition between deterministic and stochastic events , 2004, BMC Neuroscience.

[176]  A. Turing The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[177]  J. Strassmann,et al.  Altruism and social cheating in the social amoeba Dictyostelium discoideum , 2000, Nature.

[178]  S. M. Burden-Gulley,et al.  Growth cones are actively influenced by substrate-bound adhesion molecules , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[179]  B. Dickson,et al.  Comm Sorts Robo to Control Axon Guidance at the Drosophila Midline , 2002, Cell.

[180]  G. Danuser,et al.  Probing f-actin flow by tracking shape fluctuations of radial bundles in lamellipodia of motile cells. , 2000, Biophysical Journal.

[181]  M. G. Honig,et al.  Growth cones respond in diverse ways upon encountering neurites in cultures of chick dorsal root ganglia. , 1993, Developmental biology.

[182]  S. B. Kater,et al.  Laminin and fibronectin guideposts signal sustained but opposite effects to passing growth cones , 1995, Neuron.

[183]  D. Burmeister,et al.  Micropruning: the mechanism of turning of Aplysia growth cones at substrate borders in vitro , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[184]  J. Salzer,et al.  Nr-CAM and neurofascin interactions regulate ankyrin G and sodium channel clustering at the node of Ranvier , 2001, Current Biology.