Background synaptic conductance and precision of EPSP-spike coupling at pyramidal cells.

The temporal precision of converting excitatory postsynaptic potentials (EPSPs) into spikes at pyramidal cells is critical for the coding of information in the cortex. Several in vitro studies have shown that voltage-dependent conductances in pyramidal cells can prolong the EPSP time course resulting in an imprecise EPSP-spike coupling. We have used dynamic-clamp techniques to mimic the in vivo background synaptic conductance in cortical slices and investigated how the ongoing synaptic activity may affect the EPSP time course near threshold and the EPSP spike coupling. We report here that background synaptic conductance dramatically diminished the depolarization related prolongation of the EPSPs in pyramidal cells and improved the precision of spike timing. Furthermore, we found that background synaptic conductance can affect the interaction among action potentials in a spike train. Thus the level of ongoing synaptic activity in the cortex may regulate the capacity of pyramidal cells to process temporal information.

[1]  Y. Frégnac,et al.  Visual input evokes transient and strong shunting inhibition in visual cortical neurons , 1998, Nature.

[2]  T. Sejnowski,et al.  Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity , 2003, Neuroscience.

[3]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[4]  J. Lambert,et al.  Somatic amplification of distally generated subthreshold EPSPs in rat hippocampal pyramidal neurones , 1999, The Journal of physiology.

[5]  A. Destexhe,et al.  Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. , 2000, Journal of neurophysiology.

[6]  M. Häusser,et al.  Tonic Synaptic Inhibition Modulates Neuronal Output Pattern and Spatiotemporal Synaptic Integration , 1997, Neuron.

[7]  W Zieglgänsberger,et al.  Voltage dependence of excitatory postsynaptic potentials of rat neocortical neurons. , 1991, Journal of neurophysiology.

[8]  Andrea Hasenstaub,et al.  Barrages of Synaptic Activity Control the Gain and Sensitivity of Cortical Neurons , 2003, The Journal of Neuroscience.

[9]  R. Reid,et al.  Synaptic Integration in Striate Cortical Simple Cells , 1998, The Journal of Neuroscience.

[10]  H. Robinson,et al.  Postsynaptic Variability of Firing in Rat Cortical Neurons: The Roles of Input Synchronization and Synaptic NMDA Receptor Conductance , 2000, The Journal of Neuroscience.

[11]  D Contreras,et al.  Synaptic responsiveness of cortical and thalamic neurones during various phases of slow sleep oscillation in cat. , 1996, The Journal of physiology.

[12]  S. Hestrin,et al.  Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex , 1998, Nature Neuroscience.

[13]  M. Häusser,et al.  Differential shunting of EPSPs by action potentials. , 2001, Science.

[14]  S. Hestrin,et al.  Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons , 2001, Science.

[15]  M. Binder,et al.  Functional identification of the input‐output transforms of motoneurones in the rat and cat , 1997, The Journal of physiology.

[16]  O. Prospero-Garcia,et al.  Reliability of Spike Timing in Neocortical Neurons , 1995 .

[17]  E E Fetz,et al.  Relation between shapes of post‐synaptic potentials and changes in firing probability of cat motoneurones , 1983, The Journal of physiology.

[18]  E. Fetz,et al.  Synaptic Interactions between Primate Precentral Cortex Neurons Revealed by Spike-Triggered Averaging of Intracellular Membrane Potentials In Vivo , 1996, The Journal of Neuroscience.

[19]  A. Destexhe,et al.  Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons In vivo. , 1998, Journal of neurophysiology.

[20]  A. Reyes,et al.  Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons. , 1993, Journal of neurophysiology.

[21]  P. Schwindt,et al.  Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. , 1984, Journal of neurophysiology.

[22]  B. Sakmann,et al.  Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons , 1995, Neuron.

[23]  Michael J. Berry,et al.  Refractoriness and Neural Precision , 1997, The Journal of Neuroscience.

[24]  A. Destexhe,et al.  Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. , 1999, Journal of neurophysiology.

[25]  J. Donoghue,et al.  Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  Frances S. Chance,et al.  Gain Modulation from Background Synaptic Input , 2002, Neuron.

[27]  D. McCormick,et al.  Turning on and off recurrent balanced cortical activity , 2003, Nature.

[28]  M. Carandini,et al.  Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. , 2000, Journal of neurophysiology.

[29]  P. Schwindt,et al.  Modal gating of Na+ channels as a mechanism of persistent Na+ current in pyramidal neurons from rat and cat sensorimotor cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  E. Fetz,et al.  Synaptic Interactions between Cortical Neurons , 1991 .

[31]  H. Robinson,et al.  Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons , 1993, Journal of Neuroscience Methods.

[32]  Dieter Jaeger,et al.  The Contribution of NMDA and AMPA Conductances to the Control of Spiking in Neurons of the Deep Cerebellar Nuclei , 2003, The Journal of Neuroscience.

[33]  P. Schwindt,et al.  Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. , 1985, Journal of neurophysiology.

[34]  D. Ferster,et al.  Synchronous Membrane Potential Fluctuations in Neurons of the Cat Visual Cortex , 1999, Neuron.

[35]  T. Sears,et al.  The effects of single afferent impulses on the probability of firing of external intercostal motoneurones in the cat , 1982, The Journal of physiology.

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

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

[38]  R. Reid,et al.  Synchronous activity in the visual system. , 1999, Annual review of physiology.

[39]  C. Gray,et al.  Cellular Mechanisms Contributing to Response Variability of Cortical Neurons In Vivo , 1999, The Journal of Neuroscience.

[40]  R. Dingledine,et al.  Complex effects of CNQX on CA1 interneurons of the developing rat hippocampus , 2002, Neuropharmacology.

[41]  J. Hyvärinen,et al.  Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. , 1969, Journal of neurophysiology.

[42]  D. Hubel.  Single unit activity in striate cortex of unrestrained cats , 1959, The Journal of physiology.

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

[44]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[45]  C. Gray,et al.  Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  J M Bower,et al.  Synaptic Control of Spiking in Cerebellar Purkinje Cells: Dynamic Current Clamp Based on Model Conductances , 1999, The Journal of Neuroscience.

[47]  A. Grinvald,et al.  Dynamics of Ongoing Activity: Explanation of the Large Variability in Evoked Cortical Responses , 1996, Science.

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

[49]  Raymond Dingledine,et al.  Control of Feedforward Dendritic Inhibition by NMDA Receptor-Dependent Spike Timing in Hippocampal Interneurons , 2002, The Journal of Neuroscience.

[50]  Hans R. Gelderblom,et al.  Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition , 2001 .

[51]  C. Koch,et al.  Synaptic background activity influences spatiotemporal integration in single pyramidal cells. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[52]  E E Fetz,et al.  Cross‐correlation assessment of synaptic strength of single Ia fibre connections with triceps surae motoneurones in cats. , 1987, The Journal of physiology.

[53]  R. Yuste,et al.  Attractor dynamics of network UP states in the neocortex , 2003, Nature.

[54]  Stephen R. Williams,et al.  Spatial compartmentalization and functional impact of conductance in pyramidal neurons , 2004, Nature Neuroscience.

[55]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

[56]  G. Barrionuevo,et al.  Voltage-gated sodium channels shape subthreshold EPSPs in layer 5 pyramidal neurons from rat prefrontal cortex. , 2001, Journal of neurophysiology.

[57]  R. Silver,et al.  Shunting Inhibition Modulates Neuronal Gain during Synaptic Excitation , 2003, Neuron.