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TRPM8-Dependent Dynamic Response in a Mathematical Model of Cold Thermoreceptor

Author

Listed:
  • Erick Olivares
  • Simón Salgado
  • Jean Paul Maidana
  • Gaspar Herrera
  • Matías Campos
  • Rodolfo Madrid
  • Patricio Orio

Abstract

Cold-sensitive nerve terminals (CSNTs) encode steady temperatures with regular, rhythmic temperature-dependent firing patterns that range from irregular tonic firing to regular bursting (static response). During abrupt temperature changes, CSNTs show a dynamic response, transiently increasing their firing frequency as temperature decreases and silencing when the temperature increases (dynamic response). To date, mathematical models that simulate the static response are based on two depolarizing/repolarizing pairs of membrane ionic conductance (slow and fast kinetics). However, these models fail to reproduce the dynamic response of CSNTs to rapid changes in temperature and notoriously they lack a specific cold-activated conductance such as the TRPM8 channel. We developed a model that includes TRPM8 as a temperature-dependent conductance with a calcium-dependent desensitization. We show by computer simulations that it appropriately reproduces the dynamic response of CSNTs from mouse cornea, while preserving their static response behavior. In this model, the TRPM8 conductance is essential to display a dynamic response. In agreement with experimental results, TRPM8 is also needed for the ongoing activity in the absence of stimulus (i.e. neutral skin temperature). Free parameters of the model were adjusted by an evolutionary optimization algorithm, allowing us to find different solutions. We present a family of possible parameters that reproduce the behavior of CSNTs under different temperature protocols. The detection of temperature gradients is associated to a homeostatic mechanism supported by the calcium-dependent desensitization.

Suggested Citation

  • Erick Olivares & Simón Salgado & Jean Paul Maidana & Gaspar Herrera & Matías Campos & Rodolfo Madrid & Patricio Orio, 2015. "TRPM8-Dependent Dynamic Response in a Mathematical Model of Cold Thermoreceptor," PLOS ONE, Public Library of Science, vol. 10(10), pages 1-17, October.
    • Handle: RePEc:plo:pone00:0139314
    DOI: 10.1371/journal.pone.0139314
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    References listed on IDEAS

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    1. Diana M. Bautista & Jan Siemens & Joshua M. Glazer & Pamela R. Tsuruda & Allan I. Basbaum & Cheryl L. Stucky & Sven-Eric Jordt & David Julius, 2007. "The menthol receptor TRPM8 is the principal detector of environmental cold," Nature, Nature, vol. 448(7150), pages 204-208, July.
    2. X.-M. Xia & B. Fakler & A. Rivard & G. Wayman & T. Johnson-Pais & J. E. Keen & T. Ishii & B. Hirschberg & C. T. Bond & S. Lutsenko & J. Maylie & J. P. Adelman, 1998. "Mechanism of calcium gating in small-conductance calcium-activated potassium channels," Nature, Nature, vol. 395(6701), pages 503-507, October.
    3. David D. McKemy & Werner M. Neuhausser & David Julius, 2002. "Identification of a cold receptor reveals a general role for TRP channels in thermosensation," Nature, Nature, vol. 416(6876), pages 52-58, March.
    4. Thomas Voets & Guy Droogmans & Ulrich Wissenbach & Annelies Janssens & Veit Flockerzi & Bernd Nilius, 2004. "The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels," Nature, Nature, vol. 430(7001), pages 748-754, August.
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    1. Budzinski, R.C. & Boaretto, B.R.R. & Prado, T.L. & Lopes, S.R., 2019. "Temperature dependence of phase and spike synchronization of neural networks," Chaos, Solitons & Fractals, Elsevier, vol. 123(C), pages 35-42.

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