Competition in the development of nerve connections: a review of models

The establishment and refinement of neural circuits involve both the formation of new connections and the elimination of already existing connections. Elimination of connections occurs, for example, in the development of mononeural innervation of muscle fibres and in the formation of ocular dominance columns in the visual cortex. The process that leads to the elimination of connections is often referred to as axonal or synaptic competition. Although the notion of competition is commonly used, the process is not well understood - with respect to, for example, the type of competition, what axons and synapses are competing for, and the role of electrical activity. This article reviews the types of competition that have been distinguished and the models of competition that have been proposed. Models of both the neuromuscular system and the visual system are described. For each of these models, the assumptions on which it is based, its mathematical structure, and the extent to which it is supported by the experimental data are evaluated. Special attention is given to the different modelling approaches and the role of electrical activity in competition.

[1]  T Bonhoeffer,et al.  Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[2]  J. Mariani,et al.  Synapse Elimination in the Central Nervous System: Functional Significance and Cellular Mechanisms , 1996, Reviews in the neurosciences.

[3]  A. Cuello,et al.  Nerve growth factor-induced synaptogenesis and hypertrophy of cortical cholinergic terminals. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[4]  M. Werle,et al.  Elevated levels of polyneuronal innervation persist for as long as two years in reinnervated frog neuromuscular junctions. , 1991, Journal of neurobiology.

[5]  M. Moser,et al.  Making more synapses: a way to store information? , 1999, Cellular and Molecular Life Sciences CMLS.

[6]  A D Grinnell,et al.  The regulation of synaptic strength within motor units of the frog cutaneous pectoris muscle , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  N. Belluardo,et al.  Up-regulation of trkB mRNA expression in the rat striatum after seizures , 1995, Neuroscience Letters.

[8]  N. Shadbolt,et al.  Competition for Neurotrophic Factors: Ocular Dominance Columns , 1998, The Journal of Neuroscience.

[9]  R R Ribchester,et al.  Persistent polyneuronal innervation in partially denervated rat muscle after reinnervation and recovery from prolonged nerve conduction block , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Y Chen,et al.  Nerve growth factor promotes collateral sprouting of cholinergic fibers in the septohippocampal cholinergic system of aged rats with fimbria transection. , 1992, Brain research.

[11]  Edward M. Callaway,et al.  Competition favouring inactive over active motor neurons during synapse elimination , 1987, Nature.

[12]  W. Betz,et al.  The effect of selective, chronic stimulation on motor unit size in developing rat muscle , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  J. Lichtman,et al.  Synaptic Competition during the Reformation of a Neuromuscular Map , 1998, The Journal of Neuroscience.

[14]  D. Willshaw The establishment and the subsequent elimination of polyneuronal innervation of developing muscle: theoretical considerations , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[15]  F. Crépel Regression of functional synapses in the immature mammalian cerebellum , 1982, Trends in Neurosciences.

[16]  C. Malsburg,et al.  How patterned neural connections can be set up by self-organization , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[17]  C I Howarth,et al.  Axonal processes and neural plasticity. III. Competition for dendrites. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  R. Macarthur Species packing and competitive equilibrium for many species. , 1970, Theoretical population biology.

[19]  D. Purves Body and Brain: A Trophic Theory of Neural Connections , 1988 .

[20]  D J Willshaw,et al.  Development of nerve connections under the control of neurotrophic factors: parallels with consumer-resource systems in population biology. , 2000, Journal of theoretical biology.

[21]  C. Shatz,et al.  Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF , 1995, Science.

[22]  F. Richmond,et al.  Topography in the phrenic motoneuron nucleus demonstrated by retrograde multiple‐labelling techniques , 1990, The Journal of comparative neurology.

[23]  J. Sanes,et al.  Development of the vertebrate neuromuscular junction. , 1999, Annual review of neuroscience.

[24]  Peter G. H. Clarke,et al.  Mathematical Analysis of Competition Between Sensory Ganglion Cells for Nerve Growth Factor in the Skin , 1997, ICANN.

[25]  C. Gilbert Horizontal integration and cortical dynamics , 1992, Neuron.

[26]  Keiji Tanaka Organization of geniculate inputs to visual cortical cells in the cat , 1985, Vision Research.

[27]  A. V. Ooyen Activity-dependent neural network development , 1994 .

[28]  E. Callaway,et al.  Differential loss of neuromuscular connections according to activity level and spinal position of neonatal rabbit soleus motor neurons , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  P. Clarke,et al.  Retrograde neurotrophin‐mediated control of neurone survival in the developing central nervous system , 1996, Neuroreport.

[30]  W. Thompson Synapse elimination in neonatal rat muscle is sensitive to pattern of muscle use , 1983, Nature.

[31]  D. Purves,et al.  Elimination of synapses in the developing nervous system. , 1980, Science.

[32]  D. Hocking,et al.  An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  B W Festoff,et al.  Serine proteases and serpins: their possible roles in the motor system. , 1988, Revue neurologique.

[34]  Kenneth D. Miller Equivalence of a Sprouting-and-Retraction Model and Correlation-Based Plasticity Models of Neural Development , 1998, Neural Computation.

[35]  U J McMahan,et al.  Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites , 1978, The Journal of cell biology.

[36]  B G Wallace,et al.  Regulation of agrin-induced acetylcholine receptor aggregation by Ca++ and phorbol ester , 1988, The Journal of cell biology.

[37]  M. Stryker,et al.  Neural plasticity without postsynaptic action potentials: less-active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Li I. Zhang,et al.  A critical window for cooperation and competition among developing retinotectal synapses , 1998, Nature.

[39]  David J. Willshaw,et al.  The Role of Activity in Synaptic Competition at the Neuromuscular Junction , 1995, NIPS.

[40]  G Vrbová,et al.  The Role of Ca2+ in the Elimination of Polyneuronal Innervation of Rat Soleus Muscle Fibres , 1992, The European journal of neuroscience.

[41]  Randall Pittman,et al.  Cell death of motoneurons in the chick embryo spinal cord. IV. Evidence that a functional neuromuscular interaction is involved in the regulation of naturally occurring cell death and the stabilization of synapses , 1979, The Journal of comparative neurology.

[42]  S. Schuetze,et al.  Development of rat soleus endplate membrane following denervation at birth. , 1987, Journal of neurobiology.

[43]  P G Nelson,et al.  Proteolytic action of thrombin is required for electrical activity-dependent synapse reduction. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[44]  R. Ribchester,et al.  Motor unit size and synaptic competition in rat lumbrical muscles reinnervated by active and inactive motor axons. , 1983, The Journal of physiology.

[45]  J. Ma,et al.  A molecular mechanism for synapse elimination: novel inhibition of locally generated thrombin delays synapse loss in neonatal mouse muscle. , 1996, Developmental biology.

[46]  Bruno J. Ens,et al.  Models of interference and their consequences for the spatial distribution of ideal and free predators , 1997 .

[47]  Andrew Gloster,et al.  Synaptic Innervation Density Is Regulated by Neuron-Derived BDNF , 1997, Neuron.

[48]  D J Willshaw,et al.  Poly- and mononeuronal innervation in a model for the development of neuromuscular connections. , 1999, Journal of theoretical biology.

[49]  Jeff W. Lichtman,et al.  Gradual loss of synaptic cartels precedes axon withdrawal at developing neuromuscular junctions , 1993, Neuron.

[50]  U J McMahan,et al.  Reinnervation of original synaptic sites on muscle fiber basement membrane after disruption of the muscle cells. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[51]  M. R. Bennett,et al.  Growth and elimination of nerve terminals at synaptic sites during polyneuronal innervation of muscle cells: a trophic hypothesis , 1989, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[52]  R. Oppenheim,et al.  The neurotrophic theory and naturally occurring motoneuron death , 1989, Trends in Neurosciences.

[53]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  M. Stryker,et al.  Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. , 1978, The Journal of physiology.

[55]  C F Ibáñez,et al.  Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. , 1995, Science.

[56]  D. V. van Essen,et al.  Polyneuronal innervation of skeletal muscle in new‐born rats and its elimination during maturation. , 1976, The Journal of physiology.

[57]  E. Henneman The size-principle: a deterministic output emerges from a set of probabilistic connections. , 1985, The Journal of experimental biology.

[58]  M. Bothwell,et al.  Functional interactions of neurotrophins and neurotrophin receptors. , 1995, Annual review of neuroscience.

[59]  G. Vrbóva,et al.  Stabilisation of neuromuscular junctions by leupeptin increases motor unit size in partially denervated rat muscles. , 1995, Brain research. Developmental brain research.

[60]  M. Poo,et al.  Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. , 1991, Science.

[61]  R. L. Holland,et al.  Motor nerve sprouting. , 1981, Annual review of neuroscience.

[62]  P. Yodzis,et al.  Introduction to Theoretical Ecology , 1989 .

[63]  A. English,et al.  Both basic fibroblast growth factor and ciliary neurotrophic factor promote the retention of polyneuronal innervation of developing skeletal muscle fibers. , 1995, Developmental biology.

[64]  N. Swindale The development of topography in the visual cortex: a review of models. , 1996, Network.

[65]  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.

[66]  M. Gurney,et al.  Brain-derived neurotrophic factor transiently stabilizes silent synapses on developing neuromuscular junctions. , 1996, Journal of neurobiology.

[67]  M. R. Bennett,et al.  The formation of topographical maps in developing rat gastrocnemius muscle during synapse elimination. , 1988, The Journal of physiology.

[68]  L. C. Katz,et al.  Early development of ocular dominance columns. , 2000, Science.

[69]  Richard R Ribchester Cartels, competition and activity-dependent synapse elimination , 1992, Trends in Neurosciences.

[70]  J. McArdle Complex end-plate potentials at the regenerating neuromuscular junction of the rat , 1975, Experimental Neurology.

[71]  D. Anderson,et al.  Membrane depolarization induces p140trk and NGF responsiveness, but not p75LNGFR, in MAH cells. , 1992, Science.

[72]  M. Westerfield,et al.  The formation of terminal fields in the absence of competitive interactions among primary motoneurons in the zebrafish , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  M. Mazow,et al.  NGF prevents the changes induced by monocular deprivation during the critical period in rats , 1996, Brain Research.

[74]  Geoffrey J. Goodhill,et al.  Retinotectal maps: molecules, models and misplaced data , 1999, Trends in Neurosciences.

[75]  W. Webb,et al.  Lateral motion of fluorescently labeled acetylcholine receptors in membranes of developing muscle fibers. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[76]  R. O'brien,et al.  Observations on the elimination of polyneuronal innervation in developing mammalian skeletal muscle. , 1978, The Journal of physiology.

[77]  Y. Barde,et al.  Physiology of the neurotrophins. , 1996, Annual review of neuroscience.

[78]  E. Henneman Relation between size of neurons and their susceptibility to discharge. , 1957, Science.

[79]  R R Ribchester,et al.  Spatial versus consumptive competition at polyneuronally innervated neuromuscular junctions , 1994, Experimental physiology.

[80]  N. Swindale The development of topography in the visual cortex: a review of models. , 1996 .

[81]  G. Vrbóva,et al.  Non‐quantal Release of Acetylcholine Affects Polyneuronal Innervation on Developing Rat Muscle Fibres , 1993, The European journal of neuroscience.

[82]  M. Duxson,et al.  The effect of postsynaptic block on development of the neuromuscular junction in postnatal rats , 1982, Journal of neurocytology.

[83]  B. Davis,et al.  Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  J. Stollberg,et al.  Synapse elimination, the size principle, and Hebbian synapses. , 1995, Journal of neurobiology.

[85]  W. Thompson,et al.  Synaptic rearrangements and alterations in motor unit properties in neonatal rat extensor digitorum longus muscle. , 1988, The Journal of physiology.

[86]  D O Frost,et al.  BDNF Injected into the Superior Colliculus Reduces Developmental Retinal Ganglion Cell Death , 1998, The Journal of Neuroscience.

[87]  C. Shatz,et al.  Transient period of correlated bursting activity during development of the mammalian retina , 1993, Neuron.

[88]  M Holmes,et al.  Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[89]  Nigel Shadbolt,et al.  A mathematical model of activity–dependent, anatomical segregation induced by competition for neurotrophic support , 1996, Biological Cybernetics.

[90]  Yves-Alain Barde,et al.  Trophic factors and neuronal survival , 1989, Neuron.

[91]  J. Caldwell,et al.  The size of motor units during post‐natal development of rat lumbrical muscle. , 1979, The Journal of physiology.

[92]  D J Willshaw,et al.  A marker induction mechanism for the establishment of ordered neural mappings: its application to the retinotectal problem. , 1979, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[93]  M. C. Brown,et al.  Postnatal development of the adult pattern of motor axon distribution in rat muscle , 1983, Nature.

[94]  S. B. Kater,et al.  Calcium regulation of the neuronal growth cone , 1988, Trends in Neurosciences.

[95]  J. W. Lichtman,et al.  Are Neurotrophins Synaptotrophins? , 1996, Molecular and Cellular Neuroscience.

[96]  Charles Jennings,et al.  Death of a synapse , 1994, Nature.

[97]  C L Jordan,et al.  Ciliary neurotrophic factor may act in target musculature to regulate developmental synapse elimination. , 1996, Developmental neuroscience.

[98]  C. Shatz,et al.  Blockade of Endogenous Ligands of TrkB Inhibits Formation of Ocular Dominance Columns , 1997, Neuron.

[99]  Jean-Pierre Changeux,et al.  A Model for Motor Endplate Morphogenesis: Diffusible Morphogens, Transmembrane Signaling, and Compartmentalized Gene Expression , 1993, Neural Computation.

[100]  Jeff W. Lichtman,et al.  ‘Cartellian’ competition at the neuromuscular junction , 1992, Trends in Neurosciences.

[101]  Dale Purves,et al.  Geometry of neonatal neurones and the regulation of synapse elimination , 1981, Nature.

[102]  Nigel Shadbolt,et al.  Axonal Processes and Neural Plasticity: A Reply , 1998, Neural Computation.

[103]  E M Callaway,et al.  Slowing of synapse elimination by alpha-bungarotoxin superfusion of the neonatal rabbit soleus muscle. , 1989, Developmental biology.

[104]  Jeff W. Lichtman,et al.  Development of the neuromuscular junction: Genetic analysis in mice , 1998, Journal of Physiology-Paris.

[105]  K. Miller,et al.  Synaptic Economics: Competition and Cooperation in Synaptic Plasticity , 1996, Neuron.

[106]  G. Vrbová,et al.  The Effect of Inhibiting the Calcium Activated Neutral Protease, on Motor Unit Size after Partial Denervation of the Rat Soleus Muscle , 1989, The European journal of neuroscience.

[107]  Jeff W. Lichtman,et al.  Activity-Driven Synapse Elimination Leads Paradoxically to Domination by Inactive Neurons , 1999, The Journal of Neuroscience.

[108]  P. Strata,et al.  Plasticity of the olivocerebellar pathway , 1998, Trends in Neurosciences.

[109]  G. Ramakers,et al.  Depolarization stimulates lamellipodia formation and axonal but not dendritic branching in cultured rat cerebral cortex neurons. , 1998, Brain research. Developmental brain research.

[110]  Kenneth D. Miller,et al.  The Role of Constraints in Hebbian Learning , 1994, Neural Computation.

[111]  J. Jansen,et al.  The elimination of synapses in multiply-innervated skeletal muscle fibres of the rat: dependence on distance between end-plates , 1977, Brain Research.

[112]  William J. Rutter,et al.  Directed expression of NGF to pancreatic β cells in transgenic mice leads to selective hyperinnervation of the islets , 1989, Cell.

[113]  G. Turrigiano Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same , 1999, Trends in Neurosciences.

[114]  M. C. Brown,et al.  Sprouting and regression of neuromuscular synapses in partially denervated mammalian muscles. , 1978, The Journal of physiology.

[115]  E. Kandel,et al.  Structural changes accompanying memory storage. , 1993, Annual review of physiology.

[116]  Richard R. Ribchester,et al.  Competition at silent synapses in reinnervated skeletal muscle , 2000, Nature Neuroscience.

[117]  D D O'Leary,et al.  Mechanisms and molecules controlling the development of retinal maps. , 1995, Perspectives on developmental neurobiology.

[118]  T. Taxt,et al.  Local and systemic effects of tetrodotoxin on the formation and elimination of synapses in reinnervated adult rat muscle , 1983, The Journal of physiology.

[119]  M. B. Laskowski,et al.  Regeneration by skeletomotor axons in neonatal rats is topographically selective at an early stage of reinnervation , 1992, Experimental Neurology.

[120]  J. K. S. Jansen,et al.  The effect of prolonged, reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle fibers , 1979, Neuroscience.

[121]  P G Nelson,et al.  Proteolytic activity, synapse elimination, and the Hebb synapse. , 1994, Journal of neurobiology.

[122]  J. Lichtman,et al.  Axon Withdrawal during Synapse Elimination at the Neuromuscular Junction Is Accompanied by Disassembly of the Postsynaptic Specialization and Withdrawal of Schwann Cell Processes , 1998, The Journal of Neuroscience.

[123]  Yao Zhibin,et al.  Nerve growth factor promotes collateral sprouting of cholinergic fibers in the septohippocampal cholinergic system of aged rats with fimbria transection , 1992, Brain Research.

[124]  Roman Bek,et al.  Discourse on one way in which a quantum-mechanics language on the classical logical base can be built up , 1978, Kybernetika.

[125]  Thomas J. Liesegang A model of ocular dominance column development by competition for trophic factor , 1998 .

[126]  J. Donoghue Plasticity of adult sensorimotor representations , 1995, Current Opinion in Neurobiology.

[127]  J. Sanes,et al.  Topographically selective reinnervation of adult mammalian skeletal muscles , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[128]  R R Ribchester,et al.  Co‐existence and elimination of convergent motor nerve terminals in reinnervated and paralysed adult rat skeletal muscle. , 1993, The Journal of physiology.

[129]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

[130]  D. V. van Essen,et al.  Synaptic dynamics at the neuromuscular junction: mechanisms and models. , 1990, Journal of neurobiology.

[131]  H. Thoenen,et al.  Characterization of Nerve Growth Factor (NGF) Release from Hippocampal Neurons: Evidence for a Constitutive and an Unconventional Sodium‐dependent Regulated Pathway , 1995, The European journal of neuroscience.

[132]  P G Nelson,et al.  Synapse elimination from the mouse neuromuscular junction in vitro: a non-Hebbian activity-dependent process. , 1993, Journal of neurobiology.

[133]  J. Jansen,et al.  The extent of sprouting of remaining motor units in partly denervated immature and adult rat soleus muscle , 1977, Neuroscience.

[134]  Gen Sobue,et al.  Nerve growth factor enhances neurite arborization of adult sensory neurons; a study i single-cell culture , 1990, Brain Research.

[135]  L Maffei,et al.  Effects of nerve growth factor on neuronal plasticity of the kitten visual cortex. , 1993, The Journal of physiology.

[136]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[137]  Harry G. Barrow,et al.  The Role of Weight Normalization in Competitive Learning , 1994, Neural Computation.

[138]  R. Oppenheim Cell death during development of the nervous system. , 1991, Annual review of neuroscience.

[139]  M. Gurney,et al.  Leukemia inhibitory factor influences the timing of programmed synapses withdrawal from neonatal muscles. , 1995, Journal of neurobiology.

[140]  D. Willshaw,et al.  On a role for competition in the formation of patterned neural connexions , 1975, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[141]  Jeff W. Lichtman,et al.  Multiple innervation of tonic endplates revealed by activity-dependent uptake of fluorescent probes , 1985, Nature.

[142]  Niraj S. Desai,et al.  Activity-dependent scaling of quantal amplitude in neocortical neurons , 1998, Nature.

[143]  L. C. Katz,et al.  Development of ocular dominance columns in the absence of retinal input , 1999, Nature Neuroscience.

[144]  A D Grinnell,et al.  Dynamics of nerve-muscle interaction in developing and mature neuromuscular junctions. , 1995, Physiological reviews.

[145]  C I Howarth,et al.  Neural competition and statistical mechanics , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[146]  Joseph B. Long,et al.  p140 trk mRNA marks NGF-responsive forebrain neurons: Evidence that trk gene expression is induced by NGF , 1992, Neuron.

[147]  Scott E. Fraser,et al.  Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo , 1995, Nature.

[148]  W D Snider,et al.  Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. , 1998, Science.

[149]  M. Stryker Postnatal development of ocular dominance columns in layer IV of the cat's visual cortex and the effects of monocular deprivation. , 1978, Archives italiennes de biologie.

[150]  K. Miller,et al.  Ocular dominance column development: analysis and simulation. , 1989, Science.

[151]  A L Connold,et al.  Effect of low calcium and protease inhibitors on synapse elimination during postnatal development in the rat soleus muscle. , 1986, Brain research.

[152]  J. Jansen,et al.  The perinatal reorganization of the innervation of skeletal muscle in mammals , 1990, Progress in Neurobiology.

[153]  C. I. Howarth,et al.  Axonal processes and neural plasticity. II: Adult somatosensory maps. , 1996, Cerebral cortex.

[154]  D. Willshaw,et al.  Compound eyes project stripes on the optic tectum in Xenopus , 1982, Nature.

[155]  P. Clarke,et al.  Competitive exclusion between axons dependent on a single trophic substance: a mathematical analysis. , 1996, Mathematical biosciences.

[156]  N R Smalheiser,et al.  The possible role of "sibling neurite bias" in the coordination of neurite extension, branching, and survival. , 1984, Journal of neurobiology.

[157]  Nigel Shadbolt,et al.  Competition for Neurotrophic Factors: Mathematical Analysis , 1998, Neural Computation.

[158]  J. Lichtman The reorganization of synaptic connexions in the rat submandibular ganglion during post‐natal development. , 1977, The Journal of physiology.

[159]  T Magchielse,et al.  The effect of neuronal activity on the competitive elimination of neuromuscular junctions in tissue culture. , 1986, Brain research.

[160]  C. Malsburg,et al.  A mechanism for producing continuous neural mappings: ocularity dominance stripes and ordered retino , 1976 .

[161]  M. P. Stryker,et al.  The Development of Ocular Dominance Columns : Mechanisms and Models , 2003 .

[162]  R. Campenot,et al.  Development of sympathetic neurons in compartmentalized cultures. II. Local control of neurite survival by nerve growth factor. , 1982, Developmental biology.

[163]  J. Yorke,et al.  Competitive Exclusion and Nonequilibrium Coexistence , 1977, The American Naturalist.

[164]  I. Fariñas,et al.  Severe sensory and sympathetic deficits in mice lacking neurotrophin-3 , 1994, Nature.

[165]  A. V. Ooyen,et al.  Effects of Inhibition on Neural Network Development Through Activity-dependent Neurite Outgrowth , 1997 .

[166]  D. Hubel,et al.  The development of ocular dominance columns in normal and visually deprived monkeys , 1980, The Journal of comparative neurology.

[167]  J. Wolff,et al.  Synaptic reorganization in developing and adult nervous systems. , 1992, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[168]  Patrick Green S.J. Hanson and C.R. Olson (eds.), Connectionist modelling and brain function: the developing interface (MIT Press, Cambridge, MA, 1990) pp. xiii + 423, £33.75 , 1990, Biological Psychology.

[169]  L Maffei,et al.  Monocular deprivation effects in the rat visual cortex and lateral geniculate nucleus are prevented by nerve growth factor (NGF). II. Lateral geniculate nucleus , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[170]  R S Baker,et al.  Muscles of a different 'color' , 1996, Neurology.

[171]  R. Campenot,et al.  Development of sympathetic neurons in compartmentalized cultures. Il Local control of neurite growth by nerve growth factor. , 1982, Developmental biology.

[172]  T. Wiesel Postnatal development of the visual cortex and the influence of environment , 1982, Nature.

[173]  G. Carmichael,et al.  Targeted nuclear antisense RNA mimics natural antisense-induced degradation of polyoma virus early RNA. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[174]  R. Stein Nerve and Muscle: Membranes, Cells, and Systems , 1980 .

[175]  R. May,et al.  Stability and Complexity in Model Ecosystems , 1976, IEEE Transactions on Systems, Man, and Cybernetics.

[176]  M. Corner,et al.  Implications of activity dependent neurite outgrowth for neuronal morphology and network development. , 1995, Journal of theoretical biology.

[177]  Jeff W Lichtman,et al.  Mechanism of synapse disassembly at the developing neuromuscular junction , 1996, Current Opinion in Neurobiology.

[178]  Yves-Alain Barde,et al.  Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion , 1994, Nature.

[179]  E. Castrén,et al.  Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[180]  T. Lømo,et al.  What controls the development of neuromuscular junctions? , 1980, Trends in Neurosciences.

[181]  David Willshaw,et al.  The dual role of calcium in synaptic plasticity at the motor endplate , 1997 .

[182]  R. Ribchester,et al.  Repression of inactive motor nerve terminals in partially denervated rat muscle after regeneration of active motor axons. , 1984, The Journal of physiology.

[183]  Monte Westerfield,et al.  Primary Motoneurons of the Zebrafish , 1990 .

[184]  Stanley J. Wiegand,et al.  Neurotrophic factors: from molecule to man , 1994, Trends in Neurosciences.

[185]  M. Stryker,et al.  Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[186]  G E Loeb Cartels, competition and activity-dependent synapse elimination. , 1992, Trends in neurosciences.

[187]  R. Ribchester,et al.  Activity‐dependent and ‐independent synaptic interactions during reinnervation of partially denervated rat muscle. , 1988, The Journal of physiology.

[188]  J. Jansen,et al.  Postnatal loss of synaptic terminals in the partially denervated mouse soleus muscle. , 1987, Acta physiologica Scandinavica.

[189]  D. Hubel,et al.  Plasticity of ocular dominance columns in monkey striate cortex. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[190]  J. Lichtman,et al.  In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[191]  Rachel O.L. Wong,et al.  Synapse formation and elimination , 1999 .

[192]  C. I. Howarth,et al.  Axonal processes and neural plasticity.I: Ocular dominance columns. , 1996, Cerebral cortex.

[193]  A J Harris,et al.  Nerve and muscle development in paralysé mutant mice. , 1989, Developmental biology.

[194]  M. C. Brown,et al.  Short‐ and long‐term effects of paralysis on the motor innervation of two different neonatal mouse muscles , 1982, The Journal of physiology.

[195]  N. Shadbolt,et al.  A Neurotrophic Model of the Development of the Retinogeniculocortical Pathway Induced by Spontaneous Retinal Waves , 1999, The Journal of Neuroscience.

[196]  J. McManaman,et al.  Multiple Neurotrophic Factors from Skeletal Muscle: Demonstration of Effects of Basic Fibroblast Growth Factor and Comparisons with the 22‐Kilodalton Choline Acetyltransferase Development Factor , 1989, Journal of neurochemistry.