Quantal Glutamate Release Is Essential for Reliable Neuronal Encodings in Cerebral Networks

Background The neurons and synapses work coordinately to program the brain codes of controlling cognition and behaviors. Spike patterns at the presynaptic neurons regulate synaptic transmission. The quantitative regulations of synapse dynamics in spike encoding at the postsynaptic neurons remain unclear. Methodology/Principal Findings With dual whole-cell recordings at synapse-paired cells in mouse cortical slices, we have investigated the regulation of synapse dynamics to neuronal spike encoding at cerebral circuits assembled by pyramidal neurons and GABAergic ones. Our studies at unitary synapses show that postsynaptic responses are constant over time, such as glutamate receptor-channel currents at GABAergic neurons and glutamate transport currents at astrocytes, indicating quantal glutamate release. In terms of its physiological impact, our results demonstrate that the signals integrated from quantal glutamatergic synapses drive spike encoding at GABAergic neurons reliably, which in turn precisely set spike encoding at pyramidal neurons through feedback inhibition. Conclusion/Significance Our studies provide the evidences for the quantal glutamate release to drive the spike encodings precisely in cortical circuits, which may be essential for programming the reliable codes in the brain to manage well-organized behaviors.

• Publication year

  2011

• Venue

  PLoS ONE

• Publication date

  2011-09-20

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1371/journal.pone.0025219PMID 21949885PMCID 3176814
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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  2011cited by this paper
• Spike-Timing Dependent Plasticity Beyond Synapse – Pre- and Post-Synaptic Plasticity of Intrinsic Neuronal Excitability

  2010cited by this paper
• Upregulation of Barrel GABAergic Neurons Is Associated with Cross-Modal Plasticity in Olfactory Deficit

  2010cited by this paper
• Axons Amplify Somatic Incomplete Spikes into Uniform Amplitudes in Mouse Cortical Pyramidal Neurons

  2010cited by this paper
• Action potential evoked transmitter release in central synapses: insights from the developing calyx of Held

  2009cited by this paper
• The Dynamic Control of Kiss-And-Run and Vesicular Reuse Probed with Single Nanoparticles

  2009cited by this paper
• Complex brain networks: graph theoretical analysis of structural and functional systems

  2009cited by this paper
• Gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding

  2008cited by this paper
• Synaptic plasticity, memory and the hippocampus: a neural network approach to causality

  2008cited by this paper
• Homeostasis established by coordination of subcellular compartment plasticity improves spike encoding

  2008cited by this paper
• The debate on the kiss-and-run fusion at synapses.

  2007cited by this paper
• The sequence of events that underlie quantal transmission at central glutamatergic synapses

  2007cited by this paper
• Plasticity of neuronal excitability: Hebbian rules beyond the synapse.

  2007cited by this paper
• The Origin of Quantal Size Variation: Vesicular Glutamate Concentration Plays a Significant Role

  2007cited by this paper
• Intrinsic kinetics determine the time course of neuronal synaptic transporter currents.

  2006cited by this paper
• Afterhyperpolarization improves spike programming through lowering threshold potentials and refractory periods mediated by voltage-gated sodium channels.

  2006cited by this paper
• The refractory periods and threshold potentials of sequential spikes measured by whole-cell recording.

  2006cited by this paper
• Excitatory and Feed-Forward Inhibitory Hippocampal Synapses Work Synergistically as an Adaptive Filter of Natural Spike Trains

  2006cited by this paper
• Cellular signalling properties in microcircuits.

  2005cited by this paper
• Modulation of excitatory synaptic transmission by endogenous glutamate acting on presynaptic group II mGluRs in rat substantia nigra compacta

  2005cited by this paper
• Microcircuits in action--from CPGs to neocortex.

  2005cited by this paper
• Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron–principal neuron synapse

  2005cited by this paper
• Unitary IPSPs drive precise thalamic spiking in a circuit required for learning.

  2005cited by this paper
• The excitatory amino acid transporters: pharmacological insights on substrate and inhibitor specificity of the EAAT subtypes.

  2005cited by this paper
• Paired-pulse depression of unitary quantal amplitude at single hippocampal synapses.

  2004cited by this paper
• Neuronal Integration of Synaptic Input in the Fluctuation-Driven Regime

  2004cited by this paper
• Spike timing-dependent plasticity of neural circuits.

  2004cited by this paper
• Calcium signal-dependent plasticity of neuronal excitability developed postnatally.

  2004cited by this paper
• Spike Timing-Dependent Plasticity of Neural Circuits

  2004cited by this paper
• Short-term cerebral ischemia causes the dysfunction of interneurons and more excitation of pyramidal neurons in rats.

  2003cited by this paper
• Independent Sources of Quantal Variability at Single Glutamatergic Synapses

  2003cited by this paper
• Long-term plasticity of intrinsic excitability: learning rules and mechanisms.

  2003cited by this paper
• Short-term synaptic plasticity.

  2002cited by this paper
• The essence of excitation.

  2001cited by this paper
• Calcium‐calmodulin signalling pathway up‐regulates glutamatergic synaptic function in non‐pyramidal, fast spiking rat hippocampal CA1 neurons

  2001cited by this paper
• Quantal currents at single‐site central synapses

  2000cited by this paper
• The Dynamic Range for Gain Control of NMDA Receptor-Mediated Synaptic Transmission at a Single Synapse

  2000cited by this paper
• Contributions of Residual Calcium to Fast Synaptic Transmission

  1999cited by this paper
• DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters.

  1998cited by this paper
• Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures

  1998cited by this paper
• Synaptic activation of glutamate transporters in hippocampal astrocytes.

  1997cited by this paper
• Regulation of synaptic facilitation by postsynaptic Ca2+/CaM pathways in hippocampal CA1 neurons.

  1996cited by this paper
• Paired‐pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release.

  1996cited by this paper
• Exocytosis: a molecular and physiological perspective.

  1996cited by this paper
• Exocytosis: A Molecular Review and Physiological Perspective

  1996influential reference
• Amino acid neurotransmission: Dynamics of vesicular uptake

  1996cited by this paper
• Facilitation and depression at single central synapses.

  1995cited by this paper
• Changes in Presynaptic Function during Long‐Term Potentiation

  1991influential reference
• Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices.

  1990cited by this paper
• Glutamate receptor desensitization and its role in synaptic transmission.

  1989cited by this paper
• Long-term potentiation : from biophysics to behavior

  1988cited by this paper
• The current excitement in long-term potentiation.

  1988cited by this paper
• THE RELEASE OF NEURAL TRANSMITTER SUBSTANCES

  1969cited by this paper
• Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input.

  1967cited by this paper

• Modeling homosynaptic and heterosynaptic plasticity with a single neuromemristive synapse.

  2025cites this paper
• Implementation of Neuro-Memristive Synapse for Long-and Short-Term Bio-Synaptic Plasticity

  2021cites this paper
• AccessResearch Aticle Associative Memory Cells in Engram Circuits

  2019cites this paper
• Memristive Imitation of Synaptic Transmission and Plasticity

  2019cites this paper
• Plasticity of Associative Memory Cells

  2019cites this paper
• History in the Study of Learning and Memory

  2019cites this paper
• Searching basic units in memory traces: associative memory cells

  2019cites this paper
• Working Principles of Associative Memory Cells

  2019cites this paper
• Associative Memory Cells in Memory Trace

  2019cites this paper
• Associative memory cells and their working principle in the brain

  2018cites this paper
• Cell-specific plasticity associated with integrative memory of triple sensory signals in the barrel cortex

  2018cites this paper
• Functional compatibility between Purkinje cell axon branches and their target neurons in the cerebellum

  2017cites this paper
• Piriform cortical glutamatergic and GABAergic neurons express coordinated plasticity for whisker-induced odor recall

  2017cites this paper
• PKC and CaMK-II inhibitions coordinately rescue ischemia-induced GABAergic neuron dysfunction

  2017cites this paper
• Activity strengths of cortical glutamatergic and GABAergic neurons are correlated with transgenerational inheritance of learning ability

  2017cites this paper
• Ischemia deteriorates spike encoding at cortical GABAergic neurons and cerebellar Purkinje cells by increasing the intracellular Ca2.

  2017cites this paper
• Coordinated Plasticity among Glutamatergic and GABAergic Neurons and Synapses in the Barrel Cortex Is Correlated to Learning Efficiency

  2017cites this paper
• Activity-induced spontaneous spikes in GABAergic neurons suppress seizure discharges: an implication of computational modeling

  2017cites this paper
• Associative memory cells: Formation, function and perspective

  2017cites this paper
• Associative memory cells: Formation, function and perspective.

  2017cites this paper
• Inhibitions of PKC and CaMK-II synergistically rescue ischemia-induced astrocytic dysfunction.

  2017cites this paper
• Coordinated Plasticity between Barrel Cortical Glutamatergic and GABAergic Neurons during Associative Memory

  2016cites this paper
• Acidosis-Induced Dysfunction of Cortical GABAergic Neurons through Astrocyte-Related Excitotoxicity

  2015cites this paper
• A Portion of Inhibitory Neurons in Human Temporal Lobe Epilepsy are Functionally Upregulated: An Endogenous Mechanism for Seizure Termination

  2015cites this paper
• Voltage-independent sodium channels emerge for an expression of activity-induced spontaneous spikes in GABAergic neurons

  2014cites this paper
• Essential role of axonal VGSC inactivation in time-dependent deceleration and unreliability of spike propagation at cerebellar Purkinje cells

  2014cites this paper
• Long-Term Temporal Imprecision of Information Coding in the Anterior Cingulate Cortex of Mice with Peripheral Inflammation or Nerve Injury

  2014cites this paper
• The coupling features of electrical synapses modulate neuronal synchrony in hypothalamic superachiasmatic nucleus.

  2014cites this paper
• Protein Kinase C is Essential for Kainate‐Induced Anxiety‐Related Behavior and Glutamatergic Synapse Upregulation in Prelimbic Cortex

  2014cites this paper
• Cortical GABAergic neurons are more severely impaired by alkalosis than acidosis

  2013cites this paper
• Upregulation of excitatory neurons and downregulation of inhibitory neurons in barrel cortex are associated with loss of whisker inputs

  2013cites this paper
• GluR 1 , 5 activation protects cortical astrocytes and GABAergic neurons from schemia-induced impairment in

  2013cites this paper
• A sequential impairment of cortical astrocytes and GABAergic neurons during ischemia is improved by mGluR1,5 activation

  2013cites this paper
• Frequency-Dependent Reliability of Spike Propagation Is Function of Axonal Voltage-Gated Sodium Channels in Cerebellar Purkinje Cells

  2013cites this paper
• The Functional Upregulation of Piriform Cortex Is Associated with Cross-Modal Plasticity in Loss of Whisker Tactile Inputs

  2012cites this paper
• Alkalosis leads to the over-activity of cortical principal neurons.

  2012cites this paper
• Upregulation of transmitter release probability improves a conversion of synaptic analogue signals into neuronal digital spikes

  2012influential citation
• Barrel cortical neurons and astrocytes coordinately respond to an increased whisker stimulus frequency

  2012cites this paper
• mGluR1,5 activation improves network asynchrony and GABAergic synapse attenuation in the amygdala: implication for anxiety-like behavior in DBA/2 mice

  2012cites this paper
• An impairment of cortical GABAergic neurons is involved in alkalosis-induced brain dysfunctions.

  2012cites this paper
• Searching basic units in memory traces : associative memory cells [ version 1 ; peer review : awaiting peer review ]

  year unknowncites this paper