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Author Notes:

Shawn Hochman at shochm2@emory.edu

M.L.M., K.T., A.P., and S.H. designed research; M.L.M., K.T., Y.L., A.J.S., M.L.G., M.H.C., and S.H. performed research; M.L.M., K.T., A.J.S., M.L.G., and M.H.C. analyzed data; M.L.M., K.T., A.P., and S.H. wrote the paper.

The authors declare no competing financial interests.

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Research Funding:

This work was supported by the National Institutes of Health Grant 5R01NS102871 and the Department of Defense Grant SCI-30225.

M.L.M. was supported by a fellowship from the National Science Foundation (GRFP); and K.T. was supported by a fellowship from the Emory Center for Mind, Brain, and Culture (CMBC).

Keywords:

  • computational model
  • firing properties
  • membrane properties
  • mouse
  • paravertebral ganglia

Dramatically Amplified Thoracic Sympathetic Postganglionic Excitability and Integrative Capacity Revealed with Whole-Cell Patch-Clamp Recordings

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Journal Title:

eNeuro

Volume:

Volume 6, Number 2

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Type of Work:

Article | Final Publisher PDF

Abstract:

Thoracic paravertebral sympathetic postganglionic neurons (tSPNs) comprise the final integrative output of the distributed sympathetic nervous system controlling vascular and thermoregulatory systems. Considered a non-integrating relay, what little is known of tSPN intrinsic excitability has been determined by sharp microelectrodes with presumed impalement injury. We thus undertook the first electrophysiological characterization of tSPN cellular properties using whole-cell recordings and coupled results with a conductance-based model to explore the principles governing their excitability in adult mice of both sexes. Recorded membrane resistance and time constant values were an order of magnitude greater than values previously obtained, leading to a demonstrable capacity for synaptic integration in driving recruitment. Variation in membrane resistivity was the primary determinant controlling cell excitability with vastly lower currents required for tSPN recruitment. Unlike previous microelectrode recordings in mouse which observed inability to sustain firing, all tSPNs were capable of repetitive firing. Computational modeling demonstrated that observed differences are explained by introduction of a microelectrode impalement injury conductance. Overall, tSPNs largely linearly encoded injected current magnitudes over a broad frequency range with distinct subpopulations differentiable based on repetitive firing signatures. Thus, whole-cell recordings reveal tSPNs have more dramatically amplified excitability than previously thought, with greater intrinsic capacity for synaptic integration and with the ability for maintained firing to support sustained actions on vasomotor tone and thermoregulatory function. Rather than acting as a relay, these studies support a more responsive role and possible intrinsic capacity for tSPNs to drive sympathetic autonomic function.

Copyright information:

Copyright © 2019 McKinnon et al.

This is an Open Access work distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/).
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