Abstract

In vivo studies have shown that neurons in the neocortex can generate action potentials at high temporal precision. The mechanisms controlling timing and reliability of action potential generation in neocortical neurons, however, are still poorly understood. Here we investigated the temporal precision and reliability of spike firing in cortical layer V pyramidal cells at near-threshold membrane potentials. Timing and reliability of spike responses were a function of EPSC kinetics, temporal jitter of population excitatory inputs, and of background synaptic noise. We used somatic current injection to mimic population synaptic input events and measured spike probability and spike time precision (STP), the latter defined as the time window (Δt) holding 80% of response spikes. EPSC rise and decay times were varied over the known physiological spectrum. At spike threshold level, EPSC decay time had a stronger influence on STP than rise time. Generally, STP was highest (≤2.45 ms) in response to synchronous compounds of EPSCs with fast rise and decay kinetics. Compounds with slow EPSC kinetics (decay time constants>6 ms) triggered spikes at lower temporal precision (≥6.58 ms). We found an overall linear relationship between STP and spike delay. The difference in STP between fast and slow compound EPSCs could be reduced by incrementing the amplitude of slow compound EPSCs. The introduction of a temporal jitter to compound EPSCs had a comparatively small effect on STP, with a tenfold increase in jitter resulting in only a five fold decrease in STP. In the presence of simulated synaptic background activity, precisely timed spikes could still be induced by fast EPSCs, but not by slow EPSCs.

Highlights

  • BackgroundNerve cells exchange information through brief electrical signals called spikes or action potentials, which are triggered by fluctuations in the neuron’s membrane potential

  • Our findings show that the shape of postsynaptic potentials determines the temporal precision and reliability with which cortical pyramidal cells generate spikes, and how spike generation is affected by the amplitude and temporal jitter of population inputs and by the overall level of synaptic input activity

  • We have shown that the shape of postsynaptic potentials determines the temporal precision and reliability with which cortical pyramidal cells generate response spikes, and how spike generation is affected by the amplitude and temporal jitter of population inputs and by the overall level of background synaptic activity

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Summary

Background

Nerve cells exchange information through brief electrical signals called spikes or action potentials, which are triggered by fluctuations in the neuron’s membrane potential. Each spike is communicated via synapses to thousands of other neurons, causing small changes in the receiving neuron’s membrane potential called post-synaptic potentials (PSPs). Neocortical neurons receive several thousand PSPs per second, which causes their membrane potential to constantly fluctuate. Precision is influenced by noise, temporal jitter and input amplitude depends critically on the shape of EPSPs. Surprisingly, the time constant of the EPSP decay phase turned out to have the strongest influence on spike temporal precision and reliability of spike firing. The time constant of the EPSP decay phase turned out to have the strongest influence on spike temporal precision and reliability of spike firing This has interesting functional implications since the decay time constant depends on the dendritic location of the synapse and on the active and passive membrane properties of the postsynaptic neuron. Suggest that precisely timed spike patterns, at least in the close-to-threshold regime, may be preferentially communicated via proximal synaptic terminals and between neurons with small membrane time constants

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