Robustness, variability, phase dependence, and longevity of individual synaptic input effects on spike timing during fluctuating synaptic backgrounds: A modeling study of globus pallidus neuron phase response properties

N. W. Schultheiss, J. R. Edgerton, D. Jaeger

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

A neuron's phase response curve (PRC) shows how inputs arriving at different times during the spike cycle differentially affect the timing of subsequent spikes. Using a full morphological model of a globus pallidus (GP) neuron, we previously demonstrated that dendritic conductances shape the PRC in a spike frequency-dependent manner, suggesting different functional roles of perisomatic and distal dendritic synapses in the control of patterned network activity. In the present study we extend this analysis to examine the impact of physiologically realistic high conductance states on somatic and dendritic PRCs and the time course of spike train perturbations. First, we found that average somatic and dendritic PRCs preserved their shapes and spike frequency dependence when the model was driven by spatially-distributed, stochastic conductance inputs rather than tonic somatic current. However, responses to inputs during specific synaptic backgrounds often deviated substantially from the average PRC. Therefore, we analyzed the interactions of PRC stimuli with transient fluctuations in the synaptic background on a trial-by-trial basis. We found that the variability in responses to PRC stimuli and the incidence of stimulus-evoked added or skipped spikes were stimulus-phase-dependent and reflected the profile of the average PRC, suggesting commonality in the underlying mechanisms. Clear differences in the relation between the phase of input and variability of spike response between dendritic and somatic inputs indicate that these regions generally represent distinct dynamical subsystems of synaptic integration with respect to influencing the stability of spike time attractors generated by the overall synaptic conductance.

Original languageEnglish (US)
Pages (from-to)92-110
Number of pages19
JournalNeuroscience
Volume219
DOIs
StatePublished - Sep 6 2012

Bibliographical note

Funding Information:
The authors would like to thank Roberto Fernandez Galan for constructive and insightful feedback during the preparation of the manuscript. This project was supported by NINDS Grant R01NS039852 and Udall Center Grant 1P50NS071669 .

Copyright:
Copyright 2013 Elsevier B.V., All rights reserved.

Keywords

  • Dendrite
  • High conductance state
  • Phase response curve (PRC)
  • Small-conductance calcium-activated potassium (SK)
  • Spike time attractor
  • Stochastic synaptic background

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