Electrical activity and development of neural circuits

A distinct feature of the nervous system is the intricate network of synaptic connections among neurons of diverse phenotypes. Although initial connections are formed largely through molecular mechanisms that depend on intrinsic developmental programs, spontaneous and experience-driven electrical activities in the developing brain exert critical epigenetic influence on synaptic maturation and refinement of neural circuits. Selective findings discussed here illustrate some of our current understanding of the effects of electrical activity on circuit development and highlight areas that await further study.

[1]  A Pseudo-Aurora , 1911, Nature.

[2]  J. B. Ranck,et al.  Synaptic "Learning" Due to Electroosmosis: A Theory , 1964, Science.

[3]  G. Stent A physiological mechanism for Hebb's postulate of learning. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[4]  D. Hubel,et al.  Ordered arrangement of orientation columns in monkeys lacking visual experience , 1974, The Journal of comparative neurology.

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

[6]  M. Poo In situ electrophoresis of membrane components. , 1981, Annual review of biophysics and bioengineering.

[7]  T. Wiesel The postnatal development of the visual cortex and the influence of environment. , 1982, Bioscience reports.

[8]  P. Greengard,et al.  Protein phosphorylation in the brain , 1980, Nature.

[9]  J. Schmidt,et al.  Stroboscopic illumination and dark rearing block the sharpening of the regenerated retinotectal map in goldfish , 1985, Neuroscience.

[10]  M. Poo,et al.  Initial events in the formation of neuromuscular synapse: rapid induction of acetylcholine release from embryonic neuron. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[11]  L. Maffei,et al.  Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. , 1988, Science.

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

[13]  M. Poo,et al.  Diffusional and electrokinetic redistribution at the synapse: a physicochemical basis of synaptic competition. , 1990, Journal of neurobiology.

[14]  M. Constantine-Paton,et al.  Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. , 1990, Annual review of neuroscience.

[15]  D. Baylor,et al.  Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. , 1991, Science.

[16]  M. Sur,et al.  Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors , 1991, Nature.

[17]  R. Yuste,et al.  Neuronal domains in developing neocortex. , 1992, Science.

[18]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[19]  G. Mower,et al.  Brief visual experience induces immediate early gene expression in the cat visual cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Y. Dan,et al.  Hebbian depression of isolated neuromuscular synapses in vitro. , 1992, Science.

[21]  Richard Mooney,et al.  Enhancement of transmission at the developing retinogeniculate synapse , 1993, Neuron.

[22]  E. Marder,et al.  Activity-dependent changes in the intrinsic properties of cultured neurons. , 1994, Science.

[23]  Alcino J. Silva,et al.  Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein , 1994, Cell.

[24]  Jeff W. Lichtman,et al.  Long-term synapse loss induced by focal blockade of postsynaptlc receptors , 1994, Nature.

[25]  C. Shatz,et al.  Early functional neural networks in the developing retina , 1995, Nature.

[26]  R. Malinow,et al.  Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice , 1995, Nature.

[27]  M E Greenberg,et al.  Calcium signaling in neurons: molecular mechanisms and cellular consequences. , 1995, Science.

[28]  E. Villacres,et al.  Voltage-sensitive Adenylyl Cyclase Activity in Cultured Neurons. A CALCIUM-INDEPENDENT PHENOMENON (*) , 1995, The Journal of Biological Chemistry.

[29]  H. Thoenen Neurotrophins and Neuronal Plasticity , 1995, Science.

[30]  Wulfram Gerstner,et al.  A neuronal learning rule for sub-millisecond temporal coding , 1996, Nature.

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

[32]  M. Bear,et al.  Experience-dependent modification of synaptic plasticity in visual cortex , 1996, Nature.

[33]  R. Malinow,et al.  Maturation of a Central Glutamatergic Synapse , 1996, Science.

[34]  T. Bonhoeffer Neurotrophins and activity-dependent development of the neocortex , 1996, Current Opinion in Neurobiology.

[35]  V. Han,et al.  Synaptic plasticity in a cerebellum-like structure depends on temporal order , 1997, Nature.

[36]  X. Leinekugel,et al.  GABAA, NMDA and AMPA receptors: a developmentally regulated `ménage à trois' , 1997, Trends in Neurosciences.

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

[38]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[39]  M I Broder,et al.  The more things change the more they stay the same. , 1997, The American journal of medicine.

[40]  M. Weliky,et al.  Disruption of orientation tuning visual cortex by artificially correlated neuronal activity , 1997, Nature.

[41]  Michael C. Crair,et al.  Silent Synapses during Development of Thalamocortical Inputs , 1997, Neuron.

[42]  J. Lichtman,et al.  Alterations in Synaptic Strength Preceding Axon Withdrawal , 1997, Science.

[43]  D. Cooper,et al.  Regulation of Adenylyl Cyclase by Membrane Potential* , 1998, The Journal of Biological Chemistry.

[44]  Michael J. O'Donovan,et al.  Mechanisms of spontaneous activity in developing spinal networks. , 1998, Journal of neurobiology.

[45]  X Wang,et al.  Localized Synaptic Actions of Neurotrophin-4 , 1998, The Journal of Neuroscience.

[46]  M. Stryker,et al.  Comparison of Plasticity In Vivo and In Vitro in the Developing Visual Cortex of Normal and Protein Kinase A RIβ-Deficient Mice , 1998, The Journal of Neuroscience.

[47]  B. Sakmann,et al.  Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Shuh-Yow Lin,et al.  Suppression of Sprouting: An Early Function of NMDA Receptors in the Absence of AMPA/Kainate Receptor Activity , 1998, The Journal of Neuroscience.

[49]  C. Shatz,et al.  Competition in retinogeniculate patterning driven by spontaneous activity. , 1998, Science.

[50]  E. Callaway,et al.  The Development of Local, Layer-Specific Visual Cortical Axons in the Absence of Extrinsic Influences and Intrinsic Activity , 1998, The Journal of Neuroscience.

[51]  J. Kirsch,et al.  Glycine-receptor activation is required for receptor clustering in spinal neurons , 1998, Nature.

[52]  H. Cline,et al.  Promotion of dendritic growth by CPG15, an activity-induced signaling molecule. , 1998, Science.

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

[54]  C. Shatz,et al.  Regulation of Class I MHC Gene Expression in the Developing and Mature CNS by Neural Activity , 1998, Neuron.

[55]  C. Shatz,et al.  Activity-dependent cortical target selection by thalamic axons. , 1998, Science.

[56]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[57]  D. Debanne,et al.  Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures , 1998, The Journal of physiology.

[58]  R. G. Morris D.O. Hebb: The Organization of Behavior, Wiley: New York; 1949 , 1999, Brain Research Bulletin.

[59]  Mark von Zastrow,et al.  Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures , 1999, Nature Neuroscience.

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

[61]  Marco Capogna,et al.  Miniature synaptic events maintain dendritic spines via AMPA receptor activation , 1999, Nature Neuroscience.

[62]  E. Nedivi Molecular analysis of developmental plasticity in neocortex. , 1999, Journal of neurobiology.

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

[64]  K. Shen,et al.  Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. , 1999, Science.

[65]  K. Miller,et al.  Is the development of orientation selectivity instructed by activity? , 1999, Journal of neurobiology.

[66]  R. Zucker Calcium- and activity-dependent synaptic plasticity , 1999, Current Opinion in Neurobiology.

[67]  C. Shatz,et al.  Brain Waves and Brain Wiring: The Role of Endogenous and Sensory-Driven Neural Activity in Development , 1999, Pediatric Research.

[68]  E. Schuman Neurotrophin regulation of synaptic transmission , 1999, Current Opinion in Neurobiology.

[69]  M. Feller,et al.  Spontaneous Correlated Activity in Developing Neural Circuits , 1999, Neuron.

[70]  M. Weliky,et al.  Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. , 1999, Science.

[71]  Mu-ming Poo,et al.  Presynaptic depolarization facilitates neurotrophin-induced synaptic potentiation , 1999, Nature Neuroscience.

[72]  M. Constantine-Paton,et al.  The role of neural activity in synaptic development and its implications for adult brain function. , 1999, Advances in neurology.

[73]  L C Katz,et al.  Neurotrophins and synaptic plasticity. , 1999, Annual review of neuroscience.

[74]  K. Svoboda,et al.  Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. , 1999, Science.

[75]  J. A. Payne,et al.  The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation , 1999, Nature.

[76]  O. Garaschuk,et al.  Large-scale oscillatory calcium waves in the immature cortex , 2000, Nature Neuroscience.

[77]  M. Fagiolini,et al.  Inhibitory threshold for critical-period activation in primary visual cortex , 2000, Nature.

[78]  T. Südhof,et al.  Synaptic assembly of the brain in the absence of neurotransmitter secretion. , 2000, Science.

[79]  Li I. Zhang,et al.  Visual input induces long-term potentiation of developing retinotectal synapses , 2000, Nature Neuroscience.

[80]  S. Aamodt,et al.  Chronic NMDA exposure accelerates development of GABAergic inhibition in the superior colliculus. , 2000, Journal of neurophysiology.

[81]  JoAnn Buchanan,et al.  Growth cone and dendrite dynamics in zebrafish embryos: early events in synaptogenesis imaged in vivo , 2000, Nature Neuroscience.

[82]  Alessandra Angelucci,et al.  Induction of visual orientation modules in auditory cortex , 2000, Nature.

[83]  N. Spitzer,et al.  Coding of neuronal differentiation by calcium transients , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[84]  K. Svoboda,et al.  Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo , 2000, Nature.

[85]  Ivan Rodriguez,et al.  Peripheral Olfactory Projections Are Differentially Affected in Mice Deficient in a Cyclic Nucleotide-Gated Channel Subunit , 2000, Neuron.

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

[87]  C. Shatz,et al.  Functional requirement for class I MHC in CNS development and plasticity. , 2000, Science.

[88]  M. Sheng,et al.  Development of neuron–neuron synapses , 2000, Current Opinion in Neurobiology.

[89]  D. Feldman,et al.  Timing-Based LTP and LTD at Vertical Inputs to Layer II/III Pyramidal Cells in Rat Barrel Cortex , 2000, Neuron.

[90]  M. Poo,et al.  Enhancement of presynaptic neuronal excitability by correlated presynaptic and postsynaptic spiking , 2000, Nature Neuroscience.

[91]  Richard Axel,et al.  Formation of Precise Connections in the Olfactory Bulb Occurs in the Absence of Odorant-Evoked Neuronal Activity , 2000, Neuron.

[92]  T. Schwarz,et al.  Absence of Junctional Glutamate Receptor Clusters in Drosophila Mutants Lacking Spontaneous Transmitter Release , 2001, Science.

[93]  M. Bear,et al.  Visual Experience and Deprivation Bidirectionally Modify the Composition and Function of NMDA Receptors in Visual Cortex , 2001, Neuron.

[94]  Karl Deisseroth,et al.  Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology , 2001, Nature Neuroscience.

[95]  H. Cline,et al.  Dendritic arbor development and synaptogenesis , 2001, Current Opinion in Neurobiology.

[96]  Erin M. Schuman,et al.  Dynamic Visualization of Local Protein Synthesis in Hippocampal Neurons , 2001, Neuron.

[97]  B. Barres,et al.  Control of synapse number by glia. , 2001, Science.

[98]  A. Craig,et al.  Molecular heterogeneity of central synapses: afferent and target regulation , 2001, Nature Neuroscience.

[99]  Florian Engert,et al.  Emergence of Input Specificity of LTP during Development of Retinotectal Connections In Vivo , 2001, Neuron.

[100]  R. Kempter,et al.  Formation of temporal-feature maps by axonal propagation of synaptic learning , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[101]  Mu-ming Poo,et al.  Neurotrophins as synaptic modulators , 2001, Nature Reviews Neuroscience.

[102]  R. Yuste,et al.  Morphological changes in dendritic spines associated with long-term synaptic plasticity. , 2001, Annual review of neuroscience.

[103]  M. Poo,et al.  GABA Itself Promotes the Developmental Switch of Neuronal GABAergic Responses from Excitation to Inhibition , 2001, Cell.

[104]  Mu-ming Poo,et al.  Electrical Activity Modulates Growth Cone Guidance by Diffusible Factors , 2001, Neuron.

[105]  G. Bi,et al.  Synaptic modification by correlated activity: Hebb's postulate revisited. , 2001, Annual review of neuroscience.

[106]  M. Sur,et al.  Development and plasticity of cortical areas and networks , 2001, Nature Reviews Neuroscience.

[107]  Rajesh P. N. Rao,et al.  Predictive learning of temporal sequences in recurrent neocortical circuits. , 2001, Novartis Foundation symposium.

[108]  S. Aamodt,et al.  Developmental Depression of Glutamate Neurotransmission by Chronic Low-Level Activation of NMDA Receptors , 2001, The Journal of Neuroscience.

[109]  Gilles Dowek,et al.  What Is a Theory? , 2002, STACS.