Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones

Spontaneous [Ca2+]i transients were measured in the mouse neocortex from embryonic day 16 (E16) to postnatal day 6 (P6). On the day of birth (P0), cortical neurones generated widespread, highly synchronous [Ca2+]i transients over large areas. On average, 52% of neurones participated in these transients, and in 20% of slices, an average of 80% participated. These transients were blocked by TTX and nifedipine, indicating that they resulted from Ca2+ influx during electrical activity, and occurred at a mean frequency of 0.91 min−1. The occurrence of this activity was highly centred at P0: at E16 and P2 an average of only 15% and 24% of neurones, respectively, participated in synchronous transients, and they occurred at much lower frequencies at both E16 and P2 than at P0. The overall frequency of [Ca2+]i transients in individual cells did not change between E16 and P2, just the degree of their synchronicity. The onset of this spontaneous, synchronous activity correlated with a large increase in Na+ current density that occurred just before P0, and its cessation with a large decrease in resting resistance that occurred just after P2. This widespread, synchronous activity may serve a variety of functions in the neonatal nervous system.

[1]  Michael J. O'Donovan The origin of spontaneous activity in developing networks of the vertebrate nervous system , 1999, Current Opinion in Neurobiology.

[2]  L. Kaczmarek,et al.  Depolarization Selectively Increases the Expression of the Kv3.1 Potassium Channel in Developing Inferior Colliculus Neurons , 1998, The Journal of Neuroscience.

[3]  W. Moody,et al.  Na+ channel mis‐expression accelerates K+ channel development in embryonic Xenopus laevis skeletal muscle. , 1994, The Journal of physiology.

[4]  M. Stryker,et al.  Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. , 1988, Science.

[5]  M. Hanson,et al.  Depolarization and cAMP Elevation Rapidly Recruit TrkB to the Plasma Membrane of CNS Neurons , 1998, Neuron.

[6]  K R Svoboda,et al.  Activity regulates programmed cell death of zebrafish Rohon-Beard neurons. , 2001, Development.

[7]  D. O'Leary,et al.  Development, critical period plasticity, and adult reorganizations of mammalian somatosensory systems , 1994, Current Opinion in Neurobiology.

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

[9]  E. Marder,et al.  Activity-Dependent Regulation of Potassium Currents in an Identified Neuron of the Stomatogastric Ganglion of the Crab Cancer borealis , 1999, The Journal of Neuroscience.

[10]  B W Connors,et al.  Coupling between neurons of the developing rat neocortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  P. Rakic,et al.  Orchestration of neuronal migration by activity of ion channels, neurotransmitter receptors, and intracellular Ca2+ fluctuations. , 1998, Journal of neurobiology.

[12]  W. Moody,et al.  Spontaneous activity regulates calcium‐dependent K+ current expression in developing ascidian muscle , 1998, The Journal of physiology.

[13]  A. Kriegstein,et al.  Clusters of coupled neuroblasts in embryonic neocortex. , 1991, Science.

[14]  Paul Tiesinga,et al.  Influence of ionic conductances on spike timing reliability of cortical neurons for suprathreshold rhythmic inputs. , 2004, Journal of neurophysiology.

[15]  A. Ghosh,et al.  Molecular mechanisms underlying activity-dependent regulation of BDNF expression. , 1999, Journal of neurobiology.

[16]  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.

[17]  J. J. Wright,et al.  Development of Synchronized Activity of Cranial Motor Neurons in the Segmented Embryonic Mouse Hindbrain , 2003, The Journal of physiology.

[18]  J. Zhu,et al.  Maturation of layer 5 neocortical pyramidal neurons: amplifying salient layer 1 and layer 4 inputs by Ca2+ action potentials in adult rat tuft dendrites , 2000, The Journal of physiology.

[19]  Nicholas C Spitzer,et al.  Activity-dependent neuronal differentiation prior to synapse formation: the functions of calcium transients , 2002, Journal of Physiology-Paris.

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

[21]  R. Wong,et al.  Retinal waves and visual system development. , 1999, Annual review of neuroscience.

[22]  W. Moody,et al.  Action potential waveform voltage clamp shows significance of different Ca2+ channel types in developing ascidian muscle , 2000, The Journal of physiology.

[23]  P. Rakic,et al.  Selective role of N-type calcium channels in neuronal migration. , 1992, Science.

[24]  R. Yuste,et al.  Extensive dye coupling between rat neocortical neurons during the period of circuit formation , 1993, Neuron.

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

[26]  William J Moody,et al.  Early development of voltage-gated ion currents and firing properties in neurons of the mouse cerebral cortex. , 2003, Journal of neurophysiology.

[27]  H. Luhmann,et al.  Cellular physiology of the neonatal rat cerebral cortex: Intrinsic membrane properties, sodium and calcium currents , 2000, Journal of neuroscience research.

[28]  A. Draguhn,et al.  Expression of Kv1 Potassium Channels in Mouse Hippocampal Primary Cultures: Development and Activity-Dependent Regulation , 2000, The Journal of Neuroscience.

[29]  N. Spitzer,et al.  Spontaneous neuronal calcium spikes and waves during early differentiation , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  O. Garaschuk,et al.  Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus , 1998, The Journal of physiology.

[31]  Thoralf Opitz,et al.  Synchronous Oscillatory Activity in Immature Cortical Network Is Driven by GABAergic Preplate Neurons , 2001, The Journal of Neuroscience.

[32]  Y. Ben-Ari Developing networks play a similar melody , 2001, Trends in Neurosciences.

[33]  Michael J. O'Donovan,et al.  Mechanisms that initiate spontaneous network activity in the developing chick spinal cord. , 2001, Journal of neurophysiology.

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

[35]  P. Linsdell,et al.  Electrical activity and calcium influx regulate ion channel development in embryonic Xenopus skeletal muscle , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  D. O'Dowd,et al.  Differential Expression of K4-AP Currents and Kv3.1 Potassium Channel Transcripts in Cortical Neurons that Develop Distinct Firing Phenotypes , 1997, The Journal of Neuroscience.

[37]  E. Cherubini,et al.  Cyclic AMP‐dependent modulation of giant depolarizing potentials by metabotropic glutamate receptors in the rat hippocampus. , 1995, The Journal of physiology.

[38]  William J Moody,et al.  Voltage-gated currents, dye and electrical coupling in the embryonic mouse neocortex. , 2003, Cerebral cortex.

[39]  A Konnerth,et al.  Activity-dependent wiring of the developing hippocampal neuronal circuit. , 1997, Seminars in cell & developmental biology.

[40]  E. Cherubini,et al.  GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Robert M. Miura,et al.  Membrane Resonance and Stochastic Resonance Modulate Firing Patterns of Thalamocortical Neurons , 2004, Journal of Computational Neuroscience.

[42]  R. Huganir,et al.  Activation of Silent Synapses by Rapid Activity-Dependent Synaptic Recruitment of AMPA Receptors , 2001, The Journal of Neuroscience.

[43]  R. Wong,et al.  Activity-dependent regulation of dendritic growth and patterning , 2002, Nature Reviews Neuroscience.

[44]  W. Moody,et al.  Co‐ordinated modulation of Ca2+ and K+ currents during ascidian muscle development. , 1996, The Journal of physiology.

[45]  N. Spitzer,et al.  Role of calcium and protein kinase C in development of the delayed rectifier potassium current in xenopus spinal neurons , 1991, Neuron.

[46]  R. Yuste,et al.  Activity-Regulated Dynamic Behavior of Early Dendritic Protrusions: Evidence for Different Types of Dendritic Filopodia , 2003, The Journal of Neuroscience.