The role of hyperpolarization‐activated cationic current in spike‐time precision and intrinsic resonance in cortical neurons in vitro

Non‐technical summary We determined here the role of the hyperpolarization‐activated cationic (h) current on the temporal organization of hippocampal activity in vitro. In CA1 pyramidal neurons the h‐current has three main actions. In addition to setting intrinsic resonance frequency at ∼4 Hz, the h‐current determines, through two main mechanisms, the temporal precision of action potentials evoked by excitatory postsynaptic potentials or following stimulation of inhibitory postsynaptic potentials (rebound spiking). We propose that h‐channels participate in the fine tuning of oscillatory activity in hippocampal and neocortical networks.

[1]  D. Debanne,et al.  Presynaptic action potential waveform determines cortical synaptic latency , 2011, The Journal of physiology.

[2]  D. Kullmann,et al.  Ih-mediated depolarization enhances the temporal precision of neuronal integration , 2011, Nature communications.

[3]  Pierre Giraud,et al.  Spike-Time Precision and Network Synchrony Are Controlled by the Homeostatic Regulation of the D-Type Potassium Current , 2010, The Journal of Neuroscience.

[4]  E. Cherubini,et al.  Nicotine Blocks the Hyperpolarization-Activated Current Ih and Severely Impairs the Oscillatory Behavior of Oriens-Lacunosum Moleculare Interneurons , 2010, The Journal of Neuroscience.

[5]  D. Bayliss,et al.  Homeostatic Regulation of Synaptic Excitability: Tonic GABAA Receptor Currents Replace I h in Cortical Pyramidal Neurons of HCN1 Knock-Out Mice , 2010, The Journal of Neuroscience.

[6]  Lyle J. Graham,et al.  Complementary Theta Resonance Filtering by Two Spatially Segregated Mechanisms in CA1 Hippocampal Pyramidal Neurons , 2009, The Journal of Neuroscience.

[7]  Daniel Johnston,et al.  Anatomical and electrophysiological comparison of CA1 pyramidal neurons of the rat and mouse. , 2009, Journal of neurophysiology.

[8]  C. Wahl-Schott,et al.  Hyperpolarization-activated cation channels: from genes to function. , 2009, Physiological reviews.

[9]  G. Drummond Reporting ethical matters in The Journal of Physiology: standards and advice , 2009, The Journal of physiology.

[10]  Pierre Giraud,et al.  Paired-recordings from synaptically coupled cortical and hippocampal neurons in acute and cultured brain slices , 2008, Nature Protocols.

[11]  Emilie Campanac,et al.  Downregulation of Dendritic Ih in CA1 Pyramidal Neurons after LTP , 2008, The Journal of Neuroscience.

[12]  P. Somogyi,et al.  Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations , 2008, Science.

[13]  J. Lawrence,et al.  Cholinergic control of GABA release: emerging parallels between neocortex and hippocampus , 2008, Trends in Neurosciences.

[14]  D. Johnston,et al.  The h Channel Mediates Location Dependence and Plasticity of Intrinsic Phase Response in Rat Hippocampal Neurons , 2008, The Journal of Neuroscience.

[15]  D. Debanne,et al.  Release-Dependent Variations in Synaptic Latency: A Putative Code for Short- and Long-Term Synaptic Dynamics , 2007, Neuron.

[16]  Rishikesh Narayanan,et al.  Long-Term Potentiation in Rat Hippocampal Neurons Is Accompanied by Spatially Widespread Changes in Intrinsic Oscillatory Dynamics and Excitability , 2007, Neuron.

[17]  M. Nolan,et al.  HCN1 Channels Control Resting and Active Integrative Properties of Stellate Cells from Layer II of the Entorhinal Cortex , 2007, The Journal of Neuroscience.

[18]  Adriano B. L. Tort,et al.  Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy , 2007, Proceedings of the National Academy of Sciences.

[19]  John A. White,et al.  Contributions of Ih to feature selectivity in layer II stellate cells of the entorhinal cortex , 2007, Journal of Computational Neuroscience.

[20]  Pavlos Rigas,et al.  Resonance (∼10 Hz) of excitatory networks in motor cortex: effects of voltage‐dependent ion channel blockers , 2007, The Journal of physiology.

[21]  Gergo Orbán,et al.  Intrinsic and synaptic mechanisms determining the timing of neuron population activity during hippocampal theta oscillation. , 2006, Journal of neurophysiology.

[22]  D. Debanne,et al.  Metabotropic glutamate receptor subtype 1 regulates sodium currents in rat neocortical pyramidal neurons , 2006, The Journal of physiology.

[23]  Peter Jonas,et al.  Hyperpolarization‐activated cation channels in fast‐spiking interneurons of rat hippocampus , 2006, The Journal of physiology.

[24]  D. McCormick,et al.  Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential , 2006, Nature.

[25]  N. Ropert,et al.  Expression of a functional hyperpolarization-activated current (Ih) in the mouse nucleus reticularis thalami. , 2006, Journal of neurophysiology.

[26]  C. McBain,et al.  Cell type‐specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones , 2006, The Journal of physiology.

[27]  Lyle J. Graham,et al.  Contrasting Effects of the Persistent Na+ Current on Neuronal Excitability and Spike Timing , 2006, Neuron.

[28]  T. Baram,et al.  Synchronized network activity in developing rat hippocampus involves regional hyperpolarization‐activated cyclic nucleotide‐gated (HCN) channel function , 2005, The European journal of neuroscience.

[29]  R. Chitwood,et al.  Activity-dependent decrease of excitability in rat hippocampal neurons through increases in Ih , 2005, Nature Neuroscience.

[30]  Hua Hu,et al.  Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after‐hyperpolarization and excitability control in CA1 hippocampal pyramidal cells , 2005, The Journal of physiology.

[31]  Nancy Kopell,et al.  Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network. , 2005, Journal of neurophysiology.

[32]  Matthew F. Nolan,et al.  A Behavioral Role for Dendritic Integration HCN1 Channels Constrain Spatial Memory and Plasticity at Inputs to Distal Dendrites of CA1 Pyramidal Neurons , 2004, Cell.

[33]  Sheng-Nan Wu,et al.  Inhibitory Effect of Lamotrigine on A‐type Potassium Current in Hippocampal Neuron–Derived H19‐7 Cells , 2004, Epilepsia.

[34]  W. Wadman,et al.  Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization-activated Ih channels. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Eve Marder,et al.  The dynamic clamp comes of age , 2004, Trends in Neurosciences.

[36]  Nikolai Axmacher,et al.  Intrinsic cellular currents and the temporal precision of EPSP–action potential coupling in CA1 pyramidal cells , 2004, The Journal of physiology.

[37]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[38]  S. Siegelbaum,et al.  Hyperpolarization-activated cation currents: from molecules to physiological function. , 2003, Annual review of physiology.

[39]  Dominique Debanne,et al.  Long-Term Enhancement of Neuronal Excitability and Temporal Fidelity Mediated by Metabotropic Glutamate Receptor Subtype 5 , 2003, The Journal of Neuroscience.

[40]  M. Raastad,et al.  Unmyelinated axons in the rat hippocampus hyperpolarize and activate an H current when spike frequency exceeds 1 Hz , 2003, The Journal of physiology.

[41]  E. Cherubini,et al.  An Id‐like current that is downregulated by Ca2+ modulates information coding at CA3–CA3 synapses in the rat hippocampus , 2003, The Journal of physiology.

[42]  Mark Farrant,et al.  Maturation of EPSCs and Intrinsic Membrane Properties Enhances Precision at a Cerebellar Synapse , 2003, The Journal of Neuroscience.

[43]  C. Elger,et al.  Anticonvulsant pharmacology of voltage‐gated Na+ channels in hippocampal neurons of control and chronically epileptic rats , 2003, The European journal of neuroscience.

[44]  C. Davies,et al.  Activation of I h is necessary for patterning of mGluR and mAChR induced network activity in the hippocampal CA3 region , 2003, Neuropharmacology.

[45]  T. Yamauchi,et al.  The extracellular current blocking effect of cesium chloride on the theta wave in the rabbit hippocampal CA1 region , 2002, Neuroscience Letters.

[46]  J. Storm,et al.  Two forms of electrical resonance at theta frequencies, generated by M‐current, h‐current and persistent Na+ current in rat hippocampal pyramidal cells , 2002, The Journal of physiology.

[47]  Gábor Tamás,et al.  Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites , 2002, Nature Neuroscience.

[48]  D. Vasilyev,et al.  Postnatal Development of the Hyperpolarization-Activated Excitatory Current Ih in Mouse Hippocampal Pyramidal Neurons , 2002, The Journal of Neuroscience.

[49]  Fiona E. N. LeBeau,et al.  A Model of Atropine‐Resistant Theta Oscillations in Rat Hippocampal Area CA1 , 2002, The Journal of physiology.

[50]  D. Johnston,et al.  Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites , 2002, Nature Neuroscience.

[51]  P. Castillo,et al.  Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[52]  D. Ulrich,et al.  Dendritic resonance in rat neocortical pyramidal cells. , 2002, Journal of neurophysiology.

[53]  M. Scanziani,et al.  Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition , 2001, Science.

[54]  A. Hoffman,et al.  Contribution of the hyperpolarization-activated current (I(h)) to membrane potential and GABA release in hippocampal interneurons. , 2001, Journal of neurophysiology.

[55]  Ivan Soltesz,et al.  Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability , 2001, Nature Medicine.

[56]  F. G. Pike,et al.  Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents , 2000, The Journal of physiology.

[57]  Richard Miles,et al.  EPSP Amplification and the Precision of Spike Timing in Hippocampal Neurons , 2000, Neuron.

[58]  Y. Yarom,et al.  Resonance, oscillation and the intrinsic frequency preferences of neurons , 2000, Trends in Neurosciences.

[59]  M. Hasselmo,et al.  Properties and role of I(h) in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. , 2000, Journal of neurophysiology.

[60]  J. White,et al.  Channel noise in neurons , 2000, Trends in Neurosciences.

[61]  C. Chapman,et al.  Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. , 1999, Journal of neurophysiology.

[62]  J. Magee Dendritic Hyperpolarization-Activated Currents Modify the Integrative Properties of Hippocampal CA1 Pyramidal Neurons , 1998, The Journal of Neuroscience.

[63]  Idan Segev,et al.  Ion Channel Stochasticity May Be Critical in Determining the Reliability and Precision of Spike Timing , 1998, Neural Computation.

[64]  D. McCormick,et al.  H-Current Properties of a Neuronal and Network Pacemaker , 1998, Neuron.

[65]  M. MacIver,et al.  Physiology, pharmacology, and topography of cholinergic neocortical oscillations in vitro. , 1997, Journal of neurophysiology.

[66]  V. Bringuier,et al.  Synaptic origin and stimulus dependency of neuronal oscillatory activity in the primary visual cortex of the cat. , 1997, The Journal of physiology.

[67]  C. McBain,et al.  The hyperpolarization‐activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens‐alveus interneurones. , 1996, The Journal of physiology.

[68]  B. Hutcheon,et al.  Subthreshold membrane resonance in neocortical neurons. , 1996, Journal of neurophysiology.

[69]  D. McCormick,et al.  What Stops Synchronized Thalamocortical Oscillations? , 1996, Neuron.

[70]  P. Somogyi,et al.  Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons , 1995, Nature.

[71]  J. van Brederode,et al.  Differences in inhibitory synaptic input between layer II-III and layer V neurons of the cat neocortex. , 1995, Journal of neurophysiology.

[72]  Eve Marder,et al.  The dynamic clamp: artificial conductances in biological neurons , 1993, Trends in Neurosciences.

[73]  D DiFrancesco,et al.  Properties of the hyperpolarization-activated current in rat hippocampal CA1 pyramidal cells. , 1993, Journal of neurophysiology.

[74]  D. Muller,et al.  A simple method for organotypic cultures of nervous tissue , 1991, Journal of Neuroscience Methods.

[75]  R. Traub,et al.  Model of the origin of rhythmic population oscillations in the hippocampal slice. , 1989, Science.

[76]  J F Storm,et al.  An after‐hyperpolarization of medium duration in rat hippocampal pyramidal cells. , 1989, The Journal of physiology.

[77]  B. H. Bland,et al.  The development of carbachol-induced EEG ‘θ’ examined in hippocampal formation slices , 1988 .

[78]  M. Bruce MacIver,et al.  Carbachol-induced EEG ‘theta’ activity in hippocampal brain slices , 1987, Brain Research.

[79]  Daniel Johnston,et al.  Passive cable properties of hippocampal CA3 pyramidal neurons , 1981, Cellular and Molecular Neurobiology.

[80]  P. Schwartzkroin,et al.  Further characteristics of hippocampal CA1 cells in vitro , 1977, Brain Research.

[81]  D. Debanne,et al.  Axon physiology. , 2011, Physiological reviews.

[82]  H. Pape,et al.  Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. , 1996, Annual review of physiology.

[83]  J. Konopacki,et al.  The development of carbachol-induced EEG 'theta' examined in hippocampal formation slices. , 1988, Brain Research.